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Control of increasing or decreasing force during periodic isometric movement of the finger
Human Movement Science 29 (2010) 339–348
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Human Movement Science journal homepage: www.elsevier.com/locate/humov
Control of increasing or decreasing force during periodic isometric movement of the finger Junya Masumoto a, Nobuyuki Inui b,* a b
Graduate School of Education, Naruto University of Education, Naruto, Japan Laboratory of Human Motor Control, Naruto University of Education, Naruto, Japan
a r t i c l e
i n f o
PsycINFO classification: 2330 Keywords: Force variability Timing Constant error Fingertip force
a b s t r a c t The present study examined the control of force and timing during periodic isometric force production of the right index finger. Ten right-handed male participants performed three tasks cycling between lower levels (5–40%) of maximum voluntary force with a target peak-to-peak or valley-to-valley interval of 500 ms. The analysis showed that the valley force was markedly more variable than the peak force over all tasks. Participants further exhibited a greater magnitude of negative constant error at the target valley force than at the target peak force, indicating that decreasing isometric force to achieve the lower force goal resulted in underachievement of force production. This study thus confirmed that decreasing isometric force to achieve the lower force goal results in greater force variability and revealed that the linear relationship between force level and variability does not hold at lower force levels. On the other hand, the valley-to-valley interval was more variable than the peak-to-peak interval, indicating that switching from increasing force to decreasing force produced higher timing variability than switching in the opposite direction. Ó 2009 Elsevier B.V. All rights reserved.
1. Introduction Many previous studies examined the influence of force level on force variability from moderate to high force levels. For example, Schimidt, Zelaznik, Hawkins, Frank, and Quinn (1979) examined
* Corresponding author. Address: Laboratory of Human Motor Control, Course of Health and Living Sciences, Naruto University of Education, Takashima, Naruto-cho, Naruto-shi 772-8502, Japan. Tel.: +81 88 687 6517; fax: +81 88 687 6028. E-mail address: [email protected] (N. Inui). 0167-9457/$ - see front matter Ó 2009 Elsevier B.V. All rights reserved. doi:10.1016/j.humov.2009.11.006
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discrete force production over a moderate range of force levels and found that the standard deviation of force production scales linearly with force level. However, the linear relationship between force level and variability does not hold at high levels of force output although this relation has only been approximated over a moderate range of force levels (Christou, Grossman, & Carlton, 2002; Slifkin & Newell, 1999; Taylor, Christou, & Enoka, 2003). Related to this issue, Christou et al. (2002) found that there is a sigmoidal increase in the standard deviation as a function force level ranging from 5% to 95% maximal voluntary contraction (MVC) in the quadriceps femoris. They suggested that the decrease in the rate of change in variability at force levels greater than 50% MVC is the result of increments of force resulting only from motor unit discharge rate modulation. In addition, a series of studies of Enoka’s group has demonstrated that eccentric contractions are more variable than concentric contractions (for review, Christou, Tracy, & Enoka, 2002; Duchateau & Enoka, 2008). For example, Laidlaw, Bilodeau, and Enoka (2000) asked young and old adults to perform isometric and slow shortening and lengthening contractions with the first dorsal interosseous muscle. The steadiness of isometric and slow anisometric contractions was less for the old participants compared with young participants, in particular at the lower target forces and the lightest loads. Furthermore, while the variability of the lengthening contractions was greater compared with the shortening contractions for the old adults, the variability of the discharge rates of motor unit was greater for the old participants. Laidlaw et al. (2000) thus discussed that a more variable discharge by single motor units perhaps contributes to the increased ability of old adults to perform variable muscle contractions. On the other hand, Harbst, Lazarus, and Whitall (2000) examined the control of force and timing in self-paced isometric bimanual pinch tasks performed by children and adults. The participants performed a bimanual simultaneous or alternating task cycling between low levels (10–30% and 20– 40%) of MVC. Their performance was evaluated by absolute, constant, and variable errors, and these errors were divided by the value of the target force, which allowed expression of the error as a percentage of the target force. Across all ages, the participants exhibited a greater constant error at the lower target forces than at the upper targets, indicating that it is more difficult to accurately control decreasing isometric force to achieve the lower target force than it is to accurately control increasing isometric force to achieve the upper target force. Inui (2005) further asked participants to perform a bimanual finger tapping task that consisted of asymmetrical target forces (1 N and 2 N or 2 N and 4 N) at a target intertap interval of 500 ms. The analysis showed that decreasing force had a higher coefficient of variation than increasing force, regardless of the hand. Similarly, some previous studies (Hick, 1945; Spiegel, Stratton, Burke, Glendinning, & Enoka, 1996) also reported that it is more difficult to accurately control decreasing force to achieve the lower force goal than increasing isometric force to achieve the upper force goal. However, because Harbst et al. (2000) used a self-paced motor task, they did not fully examine interactions of timing and force control. In contrast, although Inui (2005) used the prescribed tapping task as an optimal method for the study of timing, the force measured by his study was not fingertip force but impact force. The present study thus confirmed that decreasing isometric force to achieve the lower force goal results in greater force variability during the periodic isometric force production and revealed that the linear relationship between force level and variability does not hold at lower force levels. Using a prescribed periodic movement interval, this study further examined the effects of increasing or decreasing force on the control of timing.
2. Method 2.1. Participants Data were obtained from 10 healthy male right-hand dominant undergraduate students (mean age: 20.5 years, SD: 0.69 years). Handedness was tested using the Edinburgh handedness inventory (Oldfield, 1971). The laterality quotients of right-handed participants were +100 overall. Informed consent for participation in the experiment was obtained from all participants.
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2.2. Procedure Participants were seated facing the load cell, and their palms rested on a support surface 6 cm above a table (see Fig. 1). From this posture, they isometrically made periodic pressing movements with the index finger of the right hand at the metacarpophalangeal joint. At the start of the experimental session, the participants produced their maximum force for 3 s to measure isometric maximum voluntary force (MVF, see Fig. 2 and Table 1). They then completed three different force production tasks: one with a peak force of 40% MVF and a valley force of 20% MVF (4020 task), a second with a peak force of 20% MVF and a valley force of 10% MVF (20-10 task) and a third with a peak force of 10% MVF and a valley force of 5% MVF (10-5 task). The target forces were determined from a previous study using 10–40% MVC (Harbst et al., 2000). First, we selected a target peak force of 20% MVF and a target valley force of 10% MVF. Second, we selected a target peak force of 10% MVF and a target valley force of 5% MVF to compare a target peak force of 10% MVF with a target valley force of the same one. Third, we selected a target peak force of 40% MVF and a target valley force of 20% MVF to compare a target peak force of 20% MVF with a target valley force of the same one. The task of the present study further consisted of a target peak-to-peak or valley-to-valley interval of 500 ms as to compare with a target intertap interval of 500 ms as often used in a finger tapping task (for example, Inui, 2005). The order of the three tasks as performed by the participants was varied randomly. They practiced each task separately with the corresponding test trial following immediately after the practice trial. They pressed their fingers against the load cell for 30 s in three practice trials for each task. During practice trials, the pressing rate was prescribed by means of an auditory metronome. The participants were instructed to synchronize finger presses on the load cell with the metronome. The output of the load cell was displayed on an oscilloscope so that they could see the difference between the realized peak or valley force and the target peak or valley force, which were indicated on the oscilloscope by two horizontal lines. If they were unable to perform the three consecutive practice trials with an average deviation from the target force of 10% or less, then practice trials were repeated two or three times. However, they were not allowed to perform more than three additional trials to avoid fatigue of the hands and fingers. On the test trial immediately after the completion of the practice trials, they pressed on the load cell for 30 s. They were instructed to produce the force and interval acquired during practice by means of self-paced movement without feedback. If they were unable to accurately produce the force according to the aforementioned criteria with regard to the average deviations in the practice trials, then the test trial was conducted once again after practice trials were repeated two or three times. In the final trial of both the practice and test trials, if the subject was unable to
Fig. 1. Experimental setup.
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Fig. 2. A data sample. An A/D converter sampled and digitized the data from the motor task for the maximum voluntary contraction after amplification and filtering.
Table 1 Maximum voluntary forces (MVFs) for the finger-pressing movement during 3 s for 10 participants. Participant
1
2
3
4
5
6
7
8
9
10
Mean
SD
MVF (N)
55.8
37.6
51.7
48.1
48.8
41.8
52.0
51.5
60.2
49.2
49.7
6.4
Abbreviations: SD: standard deviation.
accurately produce the force according to the aforementioned criteria with regard to the average deviations, their data were removed from the data analysis. 2.3. Apparatus and measurements The load cell (Model LUB-5 KB, Kyowa Electronic Instruments, Co., Tokyo, Japan; rated load = 5 kg, see Fig. 1) pressed on by participants had a nonlinearity of 0.01% rated output and a hysteresis of 0.02% rated output. When the participants synchronized their finger press on the load cell with the metronome (Model SQ100-88, Seiko Holdings Corp., Tokyo, Japan), the output of the load cell was amplified by a strain amplifier (Kyowa Model MCC-8A) and displayed on an oscilloscope (Model MD625BM-12, Leader Electronic Corp., Yokohama, Japan). The force output was also recorded on a personal computer (Apple PowerBook G4) and monitored on a screen (832 624 pixel resolution) after the amplified signal was converted from analogue to digital (PowerLab/8sp, AD Instruments). During trials, the data were sampled and digitized at a frequency of 1000 Hz by a 12 bit A/D converter after amplification and filtering at a cut-off frequency of 100 Hz. Fig. 3 shows a data sample. Peak-to-peak interval (PPI), valley-to-valley interval (VVI), time-to-peak force, and time-to-valley force were measured using the software (Emile Soft Co., Ltd., Tokushima, Japan) for analysis of interval and force (see Fig. 4). The force of each press was defined as the peak or valley output voltage from the load cell. 2.4. Statistical analysis The present study used two measures of variability of force used extensively by many previous studies: standard deviation (SD) and coefficient of variation (CV = SD/mean 100). Whereas SD is
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Fig. 3. A data sample. An A/D converter sampled and digitized the data from the prescribed motor task for the target peak force of 10% MVF, the target valley force of 5% MVF, the target peak-to-peak or valley-to-valley interval of 500 ms after amplification and filtering. Abbreviations are the same as in Table 1.
Fig. 4. The definition and measurement of dependent variables. Abbreviations: PPI, peak-to-peak interval; VVI, valley-to-valley interval.
the variability at each level of force, CV is the variability normalized by the mean level of force produced. In the analyses of the test trials, the dependent measures were the average values corresponding to the dependent measures produced. The values were calculated from 60 measures in each trial performed by each participant. In addition, constant error (CE) in the force production was calculated over 60 measures. The CE retains the sign of each error (the difference between the target and realized force production) when the average is calculated to produce an arithmetic mean error (Smyth, 1984). A 3 (Task) 2 (Force: peak force vs. valley force, interval: PPI vs. VVI or time: time-to-peak force vs. time-to-valley force) analysis of variance (ANOVA) was performed to examine the main effects on the dependent measures. When an interaction was significant, separate ANOVAs were run for peak and valley forces. When significant overall condition effects were found for a dependent measure, posthoc multiple comparisons detected differences between conditions using Tukey’s honestly significant difference. Statistical significance was defined at the p < .05 level. 3. Results To examine whether participants could match their forces across a trial for each target force, Fig. 5A shows means of both peak and valley forces (%MVF) for the 10-5, 20-10, and 40-20 tasks. The ANOVA
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on the means showed significant main effects of task (F (2, 54) = 62.94) and force (F (1, 54) = 233.60). The post-hoc test indicated that while the 10-5 task took a smaller force than both the 20-10 and 4020 tasks, the 40-20 task took a larger force than the 20-10 task. The peak force was strikingly larger than the valley force. Although separate ANOVAs on the means of peak (F (2, 27) = 34.63) and valley forces (F (2, 27) = 24.23) showed a main effect of task, the two-way interaction was significant (F (2, 54) = 11.94, p < .0001 for all cases in this paragraph). To examine variability of force for each target force, Fig. 5B and D show SDs and CVs of both peak and valley forces (%MVF) for the three tasks. SD increased as a function of force level (F (1, 54) = 22.47 p < .0001). The post-hoc test revealed that the 10-5 task was less variable than both the 20-10 (p < .05) and 40-20 (p < .0001) tasks and the 20-10 task was also less variable the 40-20 task (p < .005). The peak force was further more variable than the valley force (F (1, 54) = 7.07, p < .05). The analysis on CV also showed that the valley force was markedly more variable than the peak force (F (1, 54) = 97.14, p < .0001). However, whereas the analysis on the CV of peak force showed a main effect of task (F (2, 27) = 6.58, p < .01), that of valley force showed no main effect. The interaction of task and force was thus significant (F (2, 54) = 3.39, p < .05).
Fig. 5. Mean of both peak and valley forces (A), SD of those (B), CE of those (C) and CV of those (D) for three tasks. Abbreviations: CV, coefficient of variation; CE, constant error. Other abbreviations are the same as in Table 1.
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To further examine the accuracy of force control for each target force, Fig. 5C shows CEs of both peak and valley forces (%MVF) for the three tasks. The analysis on CE showed significant main effects of task (F (2, 54) = 3.43, p < .05) and force (F (1, 54) = 40.66, p < .0001), finding that the 40-20 task had a greater magnitude of CE than the 20-10 task (p < .05). In addition, participants exhibited greater magnitudes of negative CE at the target valley force than at the target peak force. To examine interactions of force control and timing, Fig. 6A, B, and D show means, SDs and CVs of both PPI and VVI for the three tasks. Although the analysis on the means showed no significant main effect or interaction, the analysis on both SD (F (1, 54) = 14.68, p < 0.0001) and CV (F (1, 54) = 15.58, p < .0001) showed that the VVI was more variable than the PPI. This suggested that switching from the upper target to the lower target produced a more variable interval than switching in the opposite direction. To further examine the accuracy of timing control, Fig. 6C shows CEs of both PPI and VVI for the three tasks. The analysis on CE showed a significant main effect of task (F (2, 54) = 3.07, p < .05), finding that the 10-5 task had a greater magnitude of positive CE than the 40-20 task (p < .05).
(A)
600
SD of I nterval (ms)
I nterval (ms)
450
300
150
0
10-5
20-10
(B )
80
60
40
20
0
40-20
10-5
T ask
(D) 80
60
60
CV of interval (%)
CE of interval (ms)
(C )
40
20
10-5%
20-10% T ask
40-20
T ask
80
0
20-10
40-20%
PPI VV I
40
20
0
10-5
20-10
40-20
T ask
Fig. 6. Mean of both peak-to-peak and valley-to-valley intervals (A), SD of those (B), CE of those (C) and CV of those (D) for three tasks. Abbreviations are the same as in Fig. 4 and Fig. 5.
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Figs. 7A and B show means and CVs of both time-to-peak force and time-to-valley force for the three tasks. The analysis on mean showed a significant main effect of force (F (1, 54) = 23.57, p < .0001), revealing that the time-to-peak force was longer than the time-to-valley force. The analysis on CV showed a significant main effect of task (F (2, 54) = 15.58, p < .005), indicating that the 10-5 task had more variable timing than both the 20-10 and 40-20 tasks (p < .005). 4. Discussion The main physiological observation in the present study is that the valley force was markedly more variable than the peak force over all tasks (see Fig. 5D). In other words, the force variability for a target valley force of 10% or 20% MVF was strikingly higher than that for a target peak force of the same %MVF. The 10-5 task also had more variable time to force than both the 20-10 and 40-20 tasks, indicating that force production for the smaller target force resulted in a higher variability in the time to force. Participants further exhibited greater magnitude of negative CE at the target valley force than at the target peak force (see Fig. 5C). This indicates that whereas the participants often overachieved the task for peak force production, they almost always underachieved the task for valley force production. These findings thus indicated that decreasing isometric force to achieve the lower force goal resulted in greater force variability and the underachievement of force production. As described in Section 1, when Harbst et al. (2000) examined the control of force and timing in self-paced isometric bimanual pinch tasks, participants across all ages exhibited greater magnitude of CE at the lower target forces than at the upper targets. Inui (2005) also indicated that decreasing force was more variable than increasing force in bimanual tapping tasks. Their findings were consistent with the results of the present study. This study thus corroborated that decreasing isometric force to achieve the lower force goal results in greater force variability during the periodic isometric force production with the prescribed target forces and timing. Several studies have investigated the fine control of muscle force by using feedback information (Henningsen, Knecht, & Ende-Henningsen, 1997). Because visual feedback was absent in the test trial of the present study, the fine control of isometric force may be mainly dependent of muscle spindle. Although the overall firing behavior of an agonist spindle population is proportional to the skeletomotor drive (Burke, Hagbarth, & Skuse, 1978), some of the spindles are unloaded, with the majority of primary spindles activated by the fusimotor drive in isometric muscle contractions weaker than 5–10% maximum force (Edin & Vallbo, 1990). In the present study, while the target peak force was 10%, 20%, or 40% of MVF, the target valley force was 5%, 10%, or 20% of MVF. When participants
Fig. 7. Mean of both time-to-peak force and time-to-valley force (A) and CV of those (B) for three tasks. Abbreviations are the same as in Fig. 5.
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produced the isometric force, exrafusal and intrafusal muscles perhaps contracted simultaneously using alpha–gamma coactivation and beta efferents (Pearson & Gordon, 2000). The peak force produced by coactivation of exrafusal and intrafusal muscles was stronger than the valley force, and the peak force production led to a lower percentage of unloaded spindles than the valley force production. As a result, increasing force to the upper target was more accurately controlled than decreasing force to the lower target. Enoka and his colleagues furthermore asked participants to perform shortening and lengthening contractions with the first dorsal interosseous muscle (for review, Christou et al., 2002; Duchateau & Enoka, 2008). They found that eccentric contractions are more variable than concentric contractions (Laidlaw et al., 2000) and that the fluctuations in acceleration were greater during eccentric contractions compared with concentric contractions (Christou, Shinohara, & Enoka, 2003). Whereas increases in the variabilities during concentric contractions are accompanied by an increase in the average EMG (Wessberg & Kakuda, 1999), the greater variabilities for eccentric contractions were not associated with greater muscle activity (Christou et al., 2003). At the cerebral level, despite a small EMG during lengthening contractions, the amplitude of the movement-related cortical potential derived from the electroencephalogram was greater during a lengthening contraction than a shortening contraction (Fang, Siemionow, Sahgal, Xiong, & Yue, 2001). The changes suggest that the brain is more involved in the preparation, planning, and execution of the movement and with the processing of sensory input during lengthening contractions compared with shortening contractions (Duchateau & Enoka, 2008). At the spinal level, on the other hand, the lesser EMG during an eccentric contraction when lowering a given load is attributed to a lower discharge rate and the recruitment of fewer motor units (Christova & Kossev, 2000; Laidlaw et al., 2000). The reduction in discharge rate likely includes an increased variability in discharge (Laidlaw et al., 2000), which can increase the fluctuations in the forces exerted by individual motor units (Enoka et al., 2003). Thus, the greater relative increase in the fluctuations of low-force isometric and anisometric muscle contraction and acceleration may be due to both increased discharge rate variability of the involved motor units at the spinal level and more information processing at the cerebral level. Because the latter mechanism is less evident with little report, however, the spinal mechanism at least partially contributes to the result of the present study that the valley force was markedly more variable than the peak force. Therefore, the greater increase in the variability of valley force is thought to reflect a more variable discharge rate of the motor units. Fig. 5 in the present study showed that the SD for both the peak and valley forces and the CV for the peak force monotonically increased with the mean forces, but not the CV for valley force. Many previous studies have indicated that the linear relationship between force level and variability is only approximated over a moderate range of force levels (Schmidt et al., 1979) although this relation does not hold at high levels of force output (Christou et al., 2002; Slifkin & Newell, 1999; Taylor et al., 2003). On this issue, Slifkin and Newell (1999) found that the SD of force increased exponentially as a function of force level ranging from 5% to 95% MVC in continuous force production of the index finger. They discussed that at levels up to 30–40% MVC, force is increased by adding motor unit, and beyond this level, further increases in force are achieved by increases in the discharge rate of active motor units. Except for the CV for valley force, in the current study, the SD for both the peak and valley forces and the CV for the peak force were in line with the previous studies. Sosnoff, Valantine, and Newell (2006) examined force variability at low five force levels from 0.4 N to 4 N and found that there was no change in SD at the two lowest force levels. Jones, Hamilton, and Wolpert (2002) proposed that the scaling of variability to force magnitude is due to three properties of motor unit pool: large range of twitch forces, distribution of recruitment thresholds and orderly recruitment of motor units. So Sosnoff et al. (2006) discussed that the lack of scaling of variability in the lowest force levels is due to lack of a large range of motor unit twitch forces and a distribution of recruitment thresholds. Thus, the non-linear relationship between force level and variability on CV for valley force in the current study may be due to a similar mechanism as the one proposed by Jones et al. (2002) for the lack of scaling of variability in the lowest force levels. On the other hand, the relationship between movement timing and force control has been mainly studied using a finger tapping movement. Although force control was largely independent of timing during a task of repeated isometric force production, some studies reported interactions of both parameters during periodic tapping (Billon, Semjen, & Stelmach, 1996; Keele, Ivry, & Pokorny,
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1987). For example, Sternad, Dean, and Newell (2000) identified a systematic decrease in the CV of intertap interval with specified target forces from 5 N to 15 N although the SD of intertap interval did not show any dependent on the target forces. In contrast, in the present study, both the SD and CV of both PPI and VVI did not change with specified target force although the positive CE of both the intervals decreased with increasing force levels. In the present study, however, the VVI was more variable than the PPI. Thus, although control of decreasing force to the lower target was more variable than control of increasing force to the upper target, switching from increasing force to the upper target to decreasing force to the lower target produced more variable interval than switching in the opposite direction. References Billon, M., Semjen, A., & Stelmach, G. E. (1996). The timing effects of accent production in periodic finger-tapping sequences. Journal of Motor Behavior, 28, 198–210. Burke, D., Hagbarth, K. E., & Skuse, N. F. (1978). Recruitment order of human spindle endings in isometric voluntary contractions. Journal of Physiology, 285, 101–112. Christou, E. A., Grossman, M., & Carlton, L. G. (2002). Modeling variability of force during isometric contractions of the quadriceps femoris. Journal of Motor Behavior, 34, 67–81. Christou, E. A., Shinohara, M., & Enoka, R. M. (2003). Fluctuations in acceleration during voluntary contractions lead to greater impairment of movement accuracy in old adults. Journal of Applied Physiology, 95, 373–384. Christou, E. A., Tracy, B. L., & Enoka, R. M. (2002). The steadiness of lengthening contractions. In M. L. Latash (Ed.), Progress in motor control II (pp. 195–207). Champaign, IL: Human Kinetics. Christova, P., & Kossev, A. (2000). Human motor unit activity during concentric and eccentric movement. Electromyography and Clinical Neurophysiology, 40, 331–338. Duchateau, J., & Enoka, R. M. (2008). Neural control of shortening and lengthening contraction: Influence of task constrains. Journal of Physiology, 586, 5853–5864. Edin, B. B., & Vallbo, A. B. (1990). Muscle afferent responses to isometric contractions and relaxations in humans. Journal of Neurophysiology, 63, 1307–1313. Enoka, R. M., Christou, E. A., Hunter, S. K., Kornatz, K. W., Semmler, J. G., Taylor, A. M., et al (2003). Mechanisms that contribute to differences in motor performance between young and old adults. Journal of Electromyography and Kinesiology, 13, 1–12. Fang, Y., Siemionow, W., Sahgal, V., Xiong, F., & Yue, G. H. (2001). Greater movement-related cortical potential during human eccentric versus concentric muscle contractions. Journal of Neurophysiology, 86, 1764–1772. Harbst, K. B., Lazarus, J. C., & Whitall, J. (2000). Accuracy of dynamic isometric force production: The influence of age and bimanual activation patterns. Motor Control, 4, 232–256. Henningsen, H., Knecht, S., & Ende-Henningsen, B. (1997). Influence of afferent feedback isometric fine force resolution in humans. Experimental Brain Research, 113, 207–213. Hick, W. E. (1945). The precision of incremental muscular forces with special reference to manual control design. Cambridge, UK: MRC Applied Psychological Unit. Inui, N. (2005). Coupling of force variability in bimanual tapping with asymmetrical force. Motor Control, 9, 164–179. Jones, K. E., Hamilton, A. F., & Wolpert, D. W. (2002). Sources of signal-dependent noise during isometric force production. Journal of Neurophysiology, 88, 533–544. Keele, S. W., Ivry, R. B., & Pokorny, R. A. (1987). Force control and its relation to timing. Journal of Motor Behavior, 19, 96–114. Laidlaw, D. H., Bilodeau, M., & Enoka, R. M. (2000). Steadiness is reduced and motor unit discharge is more variable in old adults. Muscle Nerve, 23, 600–612. Oldfield, R. C. (1971). The assessment and analysis of handedness: The Edinburgh inventory. Neuropsychologia, 9, 97–113. Pearson, K., & Gordon, J. (2000). Spinal reflex. In E. R. Kandel, J. H. Schwartz, & T. M. Jessell (Eds.), Principles of neural science (4th ed., pp. 713–736). New York: McGraw-Hill. Schmidt, R. A., Zelaznik, H., Hawkins, B., Frank, J. S., & Quinn, J. T. (1979). Motor-output variability: A theory for the accuracy of rapid motor acts. Psychological Review, 86, 415–451. Slifkin, A. B., & Newell, K. M. (1999). Noise, information transmission and force variability. Journal of Experimental Psychology: Human Perception and Performance, 25, 837–851. Smyth, M. M. (1984). Memory for movements. In M. M. Smyth & A. M. Wing (Eds.), The psychology of human movement (pp. 83–117). London: Academic Press. Sosnoff, J. J., Valantine, A. D., & Newell, K. M. (2006). Independence between the amount and structure of variability at low force levels. Neuroscience Letters, 392, 165–169. Spiegel, K. M., Stratton, J., Burke, J. E., Glendinning, D. S., & Enoka, R. M. (1996). The influence of age on the assessment of motor unit activation in a human hand muscle. Experimental Neurology, 81, 805–819. Sternad, D., Dean, W. J., & Newell, K. M. (2000). Force and timing variability in rhythmic unimanual tapping. Journal of Motor Behavior, 32, 249–387. Taylor, A. M., Christou, E. A., & Enoka, R. M. (2003). Multiple features of motor-unit activity influence force fluctuations during isometric contractions. Journal of Neurophysiology, 90, 1350–1361. Wessberg, J., & Kakuda, N. (1999). Single motor unit activity in relation to pulsatile motor output in human finger movements. Journal of Physiology, 517, 273–285.
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Human Movement Science journal homepage: www.elsevier.com/locate/humov
Control of increasing or decreasing force during periodic isometric movement of the finger Junya Masumoto a, Nobuyuki Inui b,* a b
Graduate School of Education, Naruto University of Education, Naruto, Japan Laboratory of Human Motor Control, Naruto University of Education, Naruto, Japan
a r t i c l e
i n f o
PsycINFO classification: 2330 Keywords: Force variability Timing Constant error Fingertip force
a b s t r a c t The present study examined the control of force and timing during periodic isometric force production of the right index finger. Ten right-handed male participants performed three tasks cycling between lower levels (5–40%) of maximum voluntary force with a target peak-to-peak or valley-to-valley interval of 500 ms. The analysis showed that the valley force was markedly more variable than the peak force over all tasks. Participants further exhibited a greater magnitude of negative constant error at the target valley force than at the target peak force, indicating that decreasing isometric force to achieve the lower force goal resulted in underachievement of force production. This study thus confirmed that decreasing isometric force to achieve the lower force goal results in greater force variability and revealed that the linear relationship between force level and variability does not hold at lower force levels. On the other hand, the valley-to-valley interval was more variable than the peak-to-peak interval, indicating that switching from increasing force to decreasing force produced higher timing variability than switching in the opposite direction. Ó 2009 Elsevier B.V. All rights reserved.
1. Introduction Many previous studies examined the influence of force level on force variability from moderate to high force levels. For example, Schimidt, Zelaznik, Hawkins, Frank, and Quinn (1979) examined
* Corresponding author. Address: Laboratory of Human Motor Control, Course of Health and Living Sciences, Naruto University of Education, Takashima, Naruto-cho, Naruto-shi 772-8502, Japan. Tel.: +81 88 687 6517; fax: +81 88 687 6028. E-mail address: [email protected] (N. Inui). 0167-9457/$ - see front matter Ó 2009 Elsevier B.V. All rights reserved. doi:10.1016/j.humov.2009.11.006
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discrete force production over a moderate range of force levels and found that the standard deviation of force production scales linearly with force level. However, the linear relationship between force level and variability does not hold at high levels of force output although this relation has only been approximated over a moderate range of force levels (Christou, Grossman, & Carlton, 2002; Slifkin & Newell, 1999; Taylor, Christou, & Enoka, 2003). Related to this issue, Christou et al. (2002) found that there is a sigmoidal increase in the standard deviation as a function force level ranging from 5% to 95% maximal voluntary contraction (MVC) in the quadriceps femoris. They suggested that the decrease in the rate of change in variability at force levels greater than 50% MVC is the result of increments of force resulting only from motor unit discharge rate modulation. In addition, a series of studies of Enoka’s group has demonstrated that eccentric contractions are more variable than concentric contractions (for review, Christou, Tracy, & Enoka, 2002; Duchateau & Enoka, 2008). For example, Laidlaw, Bilodeau, and Enoka (2000) asked young and old adults to perform isometric and slow shortening and lengthening contractions with the first dorsal interosseous muscle. The steadiness of isometric and slow anisometric contractions was less for the old participants compared with young participants, in particular at the lower target forces and the lightest loads. Furthermore, while the variability of the lengthening contractions was greater compared with the shortening contractions for the old adults, the variability of the discharge rates of motor unit was greater for the old participants. Laidlaw et al. (2000) thus discussed that a more variable discharge by single motor units perhaps contributes to the increased ability of old adults to perform variable muscle contractions. On the other hand, Harbst, Lazarus, and Whitall (2000) examined the control of force and timing in self-paced isometric bimanual pinch tasks performed by children and adults. The participants performed a bimanual simultaneous or alternating task cycling between low levels (10–30% and 20– 40%) of MVC. Their performance was evaluated by absolute, constant, and variable errors, and these errors were divided by the value of the target force, which allowed expression of the error as a percentage of the target force. Across all ages, the participants exhibited a greater constant error at the lower target forces than at the upper targets, indicating that it is more difficult to accurately control decreasing isometric force to achieve the lower target force than it is to accurately control increasing isometric force to achieve the upper target force. Inui (2005) further asked participants to perform a bimanual finger tapping task that consisted of asymmetrical target forces (1 N and 2 N or 2 N and 4 N) at a target intertap interval of 500 ms. The analysis showed that decreasing force had a higher coefficient of variation than increasing force, regardless of the hand. Similarly, some previous studies (Hick, 1945; Spiegel, Stratton, Burke, Glendinning, & Enoka, 1996) also reported that it is more difficult to accurately control decreasing force to achieve the lower force goal than increasing isometric force to achieve the upper force goal. However, because Harbst et al. (2000) used a self-paced motor task, they did not fully examine interactions of timing and force control. In contrast, although Inui (2005) used the prescribed tapping task as an optimal method for the study of timing, the force measured by his study was not fingertip force but impact force. The present study thus confirmed that decreasing isometric force to achieve the lower force goal results in greater force variability during the periodic isometric force production and revealed that the linear relationship between force level and variability does not hold at lower force levels. Using a prescribed periodic movement interval, this study further examined the effects of increasing or decreasing force on the control of timing.
2. Method 2.1. Participants Data were obtained from 10 healthy male right-hand dominant undergraduate students (mean age: 20.5 years, SD: 0.69 years). Handedness was tested using the Edinburgh handedness inventory (Oldfield, 1971). The laterality quotients of right-handed participants were +100 overall. Informed consent for participation in the experiment was obtained from all participants.
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2.2. Procedure Participants were seated facing the load cell, and their palms rested on a support surface 6 cm above a table (see Fig. 1). From this posture, they isometrically made periodic pressing movements with the index finger of the right hand at the metacarpophalangeal joint. At the start of the experimental session, the participants produced their maximum force for 3 s to measure isometric maximum voluntary force (MVF, see Fig. 2 and Table 1). They then completed three different force production tasks: one with a peak force of 40% MVF and a valley force of 20% MVF (4020 task), a second with a peak force of 20% MVF and a valley force of 10% MVF (20-10 task) and a third with a peak force of 10% MVF and a valley force of 5% MVF (10-5 task). The target forces were determined from a previous study using 10–40% MVC (Harbst et al., 2000). First, we selected a target peak force of 20% MVF and a target valley force of 10% MVF. Second, we selected a target peak force of 10% MVF and a target valley force of 5% MVF to compare a target peak force of 10% MVF with a target valley force of the same one. Third, we selected a target peak force of 40% MVF and a target valley force of 20% MVF to compare a target peak force of 20% MVF with a target valley force of the same one. The task of the present study further consisted of a target peak-to-peak or valley-to-valley interval of 500 ms as to compare with a target intertap interval of 500 ms as often used in a finger tapping task (for example, Inui, 2005). The order of the three tasks as performed by the participants was varied randomly. They practiced each task separately with the corresponding test trial following immediately after the practice trial. They pressed their fingers against the load cell for 30 s in three practice trials for each task. During practice trials, the pressing rate was prescribed by means of an auditory metronome. The participants were instructed to synchronize finger presses on the load cell with the metronome. The output of the load cell was displayed on an oscilloscope so that they could see the difference between the realized peak or valley force and the target peak or valley force, which were indicated on the oscilloscope by two horizontal lines. If they were unable to perform the three consecutive practice trials with an average deviation from the target force of 10% or less, then practice trials were repeated two or three times. However, they were not allowed to perform more than three additional trials to avoid fatigue of the hands and fingers. On the test trial immediately after the completion of the practice trials, they pressed on the load cell for 30 s. They were instructed to produce the force and interval acquired during practice by means of self-paced movement without feedback. If they were unable to accurately produce the force according to the aforementioned criteria with regard to the average deviations in the practice trials, then the test trial was conducted once again after practice trials were repeated two or three times. In the final trial of both the practice and test trials, if the subject was unable to
Fig. 1. Experimental setup.
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Fig. 2. A data sample. An A/D converter sampled and digitized the data from the motor task for the maximum voluntary contraction after amplification and filtering.
Table 1 Maximum voluntary forces (MVFs) for the finger-pressing movement during 3 s for 10 participants. Participant
1
2
3
4
5
6
7
8
9
10
Mean
SD
MVF (N)
55.8
37.6
51.7
48.1
48.8
41.8
52.0
51.5
60.2
49.2
49.7
6.4
Abbreviations: SD: standard deviation.
accurately produce the force according to the aforementioned criteria with regard to the average deviations, their data were removed from the data analysis. 2.3. Apparatus and measurements The load cell (Model LUB-5 KB, Kyowa Electronic Instruments, Co., Tokyo, Japan; rated load = 5 kg, see Fig. 1) pressed on by participants had a nonlinearity of 0.01% rated output and a hysteresis of 0.02% rated output. When the participants synchronized their finger press on the load cell with the metronome (Model SQ100-88, Seiko Holdings Corp., Tokyo, Japan), the output of the load cell was amplified by a strain amplifier (Kyowa Model MCC-8A) and displayed on an oscilloscope (Model MD625BM-12, Leader Electronic Corp., Yokohama, Japan). The force output was also recorded on a personal computer (Apple PowerBook G4) and monitored on a screen (832 624 pixel resolution) after the amplified signal was converted from analogue to digital (PowerLab/8sp, AD Instruments). During trials, the data were sampled and digitized at a frequency of 1000 Hz by a 12 bit A/D converter after amplification and filtering at a cut-off frequency of 100 Hz. Fig. 3 shows a data sample. Peak-to-peak interval (PPI), valley-to-valley interval (VVI), time-to-peak force, and time-to-valley force were measured using the software (Emile Soft Co., Ltd., Tokushima, Japan) for analysis of interval and force (see Fig. 4). The force of each press was defined as the peak or valley output voltage from the load cell. 2.4. Statistical analysis The present study used two measures of variability of force used extensively by many previous studies: standard deviation (SD) and coefficient of variation (CV = SD/mean 100). Whereas SD is
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Fig. 3. A data sample. An A/D converter sampled and digitized the data from the prescribed motor task for the target peak force of 10% MVF, the target valley force of 5% MVF, the target peak-to-peak or valley-to-valley interval of 500 ms after amplification and filtering. Abbreviations are the same as in Table 1.
Fig. 4. The definition and measurement of dependent variables. Abbreviations: PPI, peak-to-peak interval; VVI, valley-to-valley interval.
the variability at each level of force, CV is the variability normalized by the mean level of force produced. In the analyses of the test trials, the dependent measures were the average values corresponding to the dependent measures produced. The values were calculated from 60 measures in each trial performed by each participant. In addition, constant error (CE) in the force production was calculated over 60 measures. The CE retains the sign of each error (the difference between the target and realized force production) when the average is calculated to produce an arithmetic mean error (Smyth, 1984). A 3 (Task) 2 (Force: peak force vs. valley force, interval: PPI vs. VVI or time: time-to-peak force vs. time-to-valley force) analysis of variance (ANOVA) was performed to examine the main effects on the dependent measures. When an interaction was significant, separate ANOVAs were run for peak and valley forces. When significant overall condition effects were found for a dependent measure, posthoc multiple comparisons detected differences between conditions using Tukey’s honestly significant difference. Statistical significance was defined at the p < .05 level. 3. Results To examine whether participants could match their forces across a trial for each target force, Fig. 5A shows means of both peak and valley forces (%MVF) for the 10-5, 20-10, and 40-20 tasks. The ANOVA
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on the means showed significant main effects of task (F (2, 54) = 62.94) and force (F (1, 54) = 233.60). The post-hoc test indicated that while the 10-5 task took a smaller force than both the 20-10 and 4020 tasks, the 40-20 task took a larger force than the 20-10 task. The peak force was strikingly larger than the valley force. Although separate ANOVAs on the means of peak (F (2, 27) = 34.63) and valley forces (F (2, 27) = 24.23) showed a main effect of task, the two-way interaction was significant (F (2, 54) = 11.94, p < .0001 for all cases in this paragraph). To examine variability of force for each target force, Fig. 5B and D show SDs and CVs of both peak and valley forces (%MVF) for the three tasks. SD increased as a function of force level (F (1, 54) = 22.47 p < .0001). The post-hoc test revealed that the 10-5 task was less variable than both the 20-10 (p < .05) and 40-20 (p < .0001) tasks and the 20-10 task was also less variable the 40-20 task (p < .005). The peak force was further more variable than the valley force (F (1, 54) = 7.07, p < .05). The analysis on CV also showed that the valley force was markedly more variable than the peak force (F (1, 54) = 97.14, p < .0001). However, whereas the analysis on the CV of peak force showed a main effect of task (F (2, 27) = 6.58, p < .01), that of valley force showed no main effect. The interaction of task and force was thus significant (F (2, 54) = 3.39, p < .05).
Fig. 5. Mean of both peak and valley forces (A), SD of those (B), CE of those (C) and CV of those (D) for three tasks. Abbreviations: CV, coefficient of variation; CE, constant error. Other abbreviations are the same as in Table 1.
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To further examine the accuracy of force control for each target force, Fig. 5C shows CEs of both peak and valley forces (%MVF) for the three tasks. The analysis on CE showed significant main effects of task (F (2, 54) = 3.43, p < .05) and force (F (1, 54) = 40.66, p < .0001), finding that the 40-20 task had a greater magnitude of CE than the 20-10 task (p < .05). In addition, participants exhibited greater magnitudes of negative CE at the target valley force than at the target peak force. To examine interactions of force control and timing, Fig. 6A, B, and D show means, SDs and CVs of both PPI and VVI for the three tasks. Although the analysis on the means showed no significant main effect or interaction, the analysis on both SD (F (1, 54) = 14.68, p < 0.0001) and CV (F (1, 54) = 15.58, p < .0001) showed that the VVI was more variable than the PPI. This suggested that switching from the upper target to the lower target produced a more variable interval than switching in the opposite direction. To further examine the accuracy of timing control, Fig. 6C shows CEs of both PPI and VVI for the three tasks. The analysis on CE showed a significant main effect of task (F (2, 54) = 3.07, p < .05), finding that the 10-5 task had a greater magnitude of positive CE than the 40-20 task (p < .05).
(A)
600
SD of I nterval (ms)
I nterval (ms)
450
300
150
0
10-5
20-10
(B )
80
60
40
20
0
40-20
10-5
T ask
(D) 80
60
60
CV of interval (%)
CE of interval (ms)
(C )
40
20
10-5%
20-10% T ask
40-20
T ask
80
0
20-10
40-20%
PPI VV I
40
20
0
10-5
20-10
40-20
T ask
Fig. 6. Mean of both peak-to-peak and valley-to-valley intervals (A), SD of those (B), CE of those (C) and CV of those (D) for three tasks. Abbreviations are the same as in Fig. 4 and Fig. 5.
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Figs. 7A and B show means and CVs of both time-to-peak force and time-to-valley force for the three tasks. The analysis on mean showed a significant main effect of force (F (1, 54) = 23.57, p < .0001), revealing that the time-to-peak force was longer than the time-to-valley force. The analysis on CV showed a significant main effect of task (F (2, 54) = 15.58, p < .005), indicating that the 10-5 task had more variable timing than both the 20-10 and 40-20 tasks (p < .005). 4. Discussion The main physiological observation in the present study is that the valley force was markedly more variable than the peak force over all tasks (see Fig. 5D). In other words, the force variability for a target valley force of 10% or 20% MVF was strikingly higher than that for a target peak force of the same %MVF. The 10-5 task also had more variable time to force than both the 20-10 and 40-20 tasks, indicating that force production for the smaller target force resulted in a higher variability in the time to force. Participants further exhibited greater magnitude of negative CE at the target valley force than at the target peak force (see Fig. 5C). This indicates that whereas the participants often overachieved the task for peak force production, they almost always underachieved the task for valley force production. These findings thus indicated that decreasing isometric force to achieve the lower force goal resulted in greater force variability and the underachievement of force production. As described in Section 1, when Harbst et al. (2000) examined the control of force and timing in self-paced isometric bimanual pinch tasks, participants across all ages exhibited greater magnitude of CE at the lower target forces than at the upper targets. Inui (2005) also indicated that decreasing force was more variable than increasing force in bimanual tapping tasks. Their findings were consistent with the results of the present study. This study thus corroborated that decreasing isometric force to achieve the lower force goal results in greater force variability during the periodic isometric force production with the prescribed target forces and timing. Several studies have investigated the fine control of muscle force by using feedback information (Henningsen, Knecht, & Ende-Henningsen, 1997). Because visual feedback was absent in the test trial of the present study, the fine control of isometric force may be mainly dependent of muscle spindle. Although the overall firing behavior of an agonist spindle population is proportional to the skeletomotor drive (Burke, Hagbarth, & Skuse, 1978), some of the spindles are unloaded, with the majority of primary spindles activated by the fusimotor drive in isometric muscle contractions weaker than 5–10% maximum force (Edin & Vallbo, 1990). In the present study, while the target peak force was 10%, 20%, or 40% of MVF, the target valley force was 5%, 10%, or 20% of MVF. When participants
Fig. 7. Mean of both time-to-peak force and time-to-valley force (A) and CV of those (B) for three tasks. Abbreviations are the same as in Fig. 5.
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produced the isometric force, exrafusal and intrafusal muscles perhaps contracted simultaneously using alpha–gamma coactivation and beta efferents (Pearson & Gordon, 2000). The peak force produced by coactivation of exrafusal and intrafusal muscles was stronger than the valley force, and the peak force production led to a lower percentage of unloaded spindles than the valley force production. As a result, increasing force to the upper target was more accurately controlled than decreasing force to the lower target. Enoka and his colleagues furthermore asked participants to perform shortening and lengthening contractions with the first dorsal interosseous muscle (for review, Christou et al., 2002; Duchateau & Enoka, 2008). They found that eccentric contractions are more variable than concentric contractions (Laidlaw et al., 2000) and that the fluctuations in acceleration were greater during eccentric contractions compared with concentric contractions (Christou, Shinohara, & Enoka, 2003). Whereas increases in the variabilities during concentric contractions are accompanied by an increase in the average EMG (Wessberg & Kakuda, 1999), the greater variabilities for eccentric contractions were not associated with greater muscle activity (Christou et al., 2003). At the cerebral level, despite a small EMG during lengthening contractions, the amplitude of the movement-related cortical potential derived from the electroencephalogram was greater during a lengthening contraction than a shortening contraction (Fang, Siemionow, Sahgal, Xiong, & Yue, 2001). The changes suggest that the brain is more involved in the preparation, planning, and execution of the movement and with the processing of sensory input during lengthening contractions compared with shortening contractions (Duchateau & Enoka, 2008). At the spinal level, on the other hand, the lesser EMG during an eccentric contraction when lowering a given load is attributed to a lower discharge rate and the recruitment of fewer motor units (Christova & Kossev, 2000; Laidlaw et al., 2000). The reduction in discharge rate likely includes an increased variability in discharge (Laidlaw et al., 2000), which can increase the fluctuations in the forces exerted by individual motor units (Enoka et al., 2003). Thus, the greater relative increase in the fluctuations of low-force isometric and anisometric muscle contraction and acceleration may be due to both increased discharge rate variability of the involved motor units at the spinal level and more information processing at the cerebral level. Because the latter mechanism is less evident with little report, however, the spinal mechanism at least partially contributes to the result of the present study that the valley force was markedly more variable than the peak force. Therefore, the greater increase in the variability of valley force is thought to reflect a more variable discharge rate of the motor units. Fig. 5 in the present study showed that the SD for both the peak and valley forces and the CV for the peak force monotonically increased with the mean forces, but not the CV for valley force. Many previous studies have indicated that the linear relationship between force level and variability is only approximated over a moderate range of force levels (Schmidt et al., 1979) although this relation does not hold at high levels of force output (Christou et al., 2002; Slifkin & Newell, 1999; Taylor et al., 2003). On this issue, Slifkin and Newell (1999) found that the SD of force increased exponentially as a function of force level ranging from 5% to 95% MVC in continuous force production of the index finger. They discussed that at levels up to 30–40% MVC, force is increased by adding motor unit, and beyond this level, further increases in force are achieved by increases in the discharge rate of active motor units. Except for the CV for valley force, in the current study, the SD for both the peak and valley forces and the CV for the peak force were in line with the previous studies. Sosnoff, Valantine, and Newell (2006) examined force variability at low five force levels from 0.4 N to 4 N and found that there was no change in SD at the two lowest force levels. Jones, Hamilton, and Wolpert (2002) proposed that the scaling of variability to force magnitude is due to three properties of motor unit pool: large range of twitch forces, distribution of recruitment thresholds and orderly recruitment of motor units. So Sosnoff et al. (2006) discussed that the lack of scaling of variability in the lowest force levels is due to lack of a large range of motor unit twitch forces and a distribution of recruitment thresholds. Thus, the non-linear relationship between force level and variability on CV for valley force in the current study may be due to a similar mechanism as the one proposed by Jones et al. (2002) for the lack of scaling of variability in the lowest force levels. On the other hand, the relationship between movement timing and force control has been mainly studied using a finger tapping movement. Although force control was largely independent of timing during a task of repeated isometric force production, some studies reported interactions of both parameters during periodic tapping (Billon, Semjen, & Stelmach, 1996; Keele, Ivry, & Pokorny,
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1987). For example, Sternad, Dean, and Newell (2000) identified a systematic decrease in the CV of intertap interval with specified target forces from 5 N to 15 N although the SD of intertap interval did not show any dependent on the target forces. In contrast, in the present study, both the SD and CV of both PPI and VVI did not change with specified target force although the positive CE of both the intervals decreased with increasing force levels. In the present study, however, the VVI was more variable than the PPI. Thus, although control of decreasing force to the lower target was more variable than control of increasing force to the upper target, switching from increasing force to the upper target to decreasing force to the lower target produced more variable interval than switching in the opposite direction. References Billon, M., Semjen, A., & Stelmach, G. E. (1996). The timing effects of accent production in periodic finger-tapping sequences. 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