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Asymmetric control of force and symmetric control of timing in bimanual finger tapping
Human Movement Science 21 (2002) 131–146 www.elsevier.com/locate/humov
Asymmetric control of force and symmetric control of timing in bimanual finger tapping Nobuyuki Inui a
a,*
, Hiroshi Hatta
b
Department of Human Motor Control, Faculty of Health and Living Sciences, Naruto University of Education, Takashima, Naruto-cho, Naruto-shi 772-8502, Japan b Graduate School of Education, Naruto University of Education, Takashima, Naruto-cho, Naruto-shi 772-8502, Japan Accepted 27 March 2002
Abstract An experiment was conducted to examine the control of force and timing in bimanual finger tapping. Participants were trained to produce both unimanual (left or right hand) and bimanual finger-tapping sequences with a peak force of 200 g and an intertap interval (ITI) of 400 ms. During practice, visual force feedback was provided pertaining to the hand performing the unimanual tapping sequences and to either the dominant or the nondominant hand in the bimanual tapping sequences. After practice, the participants produced the learned unimanual and bimanual tapping sequences in the absence of feedback. In those trials the force produced by the dominant (right) hand was significantly larger than that produced by the nondominant (left) hand, in the absence of a significant difference between the ITIs produced by both hands. Furthermore, after unilateral feedback had been provided of the force produced by the nondominant hand, the force output of the dominant hand was significantly more variable than that of the nondominant hand. In contrast, after feedback had been provided of the force produced by the dominant hand, the variability of the force outputs of the two hands did not differ significantly. These results were discussed in the light of both neurophysiological and anatomical findings, and were interpreted to imply that the control of timing (in bimanual tasks) may be more tightly coupled in the motor system than the control of force. Ó 2002 Elsevier Science B.V. All rights reserved.
*
Corresponding author. Tel.: +81-088-684-6517; fax: +81-088-687-6028. E-mail address: [email protected] (N. Inui).
0167-9457/02/$ - see front matter Ó 2002 Elsevier Science B.V. All rights reserved. PII: S 0 1 6 7 - 9 4 5 7 ( 0 2 ) 0 0 0 9 4 - 5
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PsycINFO classification: 2330 Keywords: Force control; Movement timing; Bimanual tapping
1. Introduction In the last two decades, the coordination between bimanual rhythmic movements has been studied extensively in experiments using finger oscillations (Kelso, 1984), finger tapping (Yamanishi, Kawato, & Suzuki, 1980), wrist rotations (Carson, Byblow, & Goodman, 1994), and whole arm movements (Swinnen & Walter, 1991). Persistent and robust findings in this line of research have been that: (1) in-phase (simultaneous) and antiphase (alternating) movements are the only phase relations that are stable and easy to achieve without practice (Yamanishi et al., 1980); (2) in-phase movements are more stable than antiphase movements (Scholz & Kelso, 1990), and (3) the stability of in-phase and antiphase movements decreases with increasing movement frequency (Post, Peper, & Beek, 2000). However, these studies on bimanual rhythmic movements typically focus on kinematical measures only. To date, the ability to coordinate rhythmic bimanual movements with kinetic measures has seldom been studied ða notable exception is a recent study by Peper and Carson (1999)Þ. Nevertheless, it may be argued that, in order to develop a more complete understanding of bimanual coordination, it is essential to examine how both timing and force production of bimanual hand movements are controlled. Like timing and relative phasing, isometric force production has been studied extensively in bimanual tasks. Henry and Smith (1961) found that the maximal force that can be produced by each hand in a bimanual grip task is less than the maximal force that can be produced by each hand separately. This bilateral deficit was also reported using static flexion of the wrist (Kroll, 1965) and static extension of the leg (Secher, Rorsgaard, & Secher, 1978). Using a static grip and a static flexion and extension of the elbow, in combination with EMG recordings, Ohtsuki (1994) found that besides the bilateral deficit, the reaction time of simultaneous bimanual responses is longer than that of unimanual responses. To identify the mechanisms underlying the bilateral deficit, Taniguchi, Burle, Vidal, and Bonnet (2001) examined an electroencephalographic correlate of the bilateral deficit during the preparation and execution stages of a reaction-time task. They found that the activation of the sensorimotor area of the right hand directly involved in voluntary control is weaker for bilateral than for unilateral contralateral responses. On the basis of this finding, they hypothesized that a transcallosal inhibitory effect persists in the bilateral response. In young children, the intentional production of force in one hand is accompanied by the unintentional production of force in the other hand (Lazarus & Todor, 1987; Todor & Lazarus, 1986). Although the unintentionally produced force is much smaller than the intentionally produced force, the similarity in the patterns of force production evidences that the control of manual force output is coupled in the immature human motor system. Henningsen, Ende-Henningsen, and Gordon (1995) examined the ability of adults to match the voluntary isometric finger flexion forces of the
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dominant with those of the nondominant hand, and found that larger forces were exerted with the index finger of the dominant hand. This finding suggests the presence of asymmetrical hemispheric thresholds for hand muscle activation, as well as an asymmetrical regional blood flow in the primary motor and premotor areas during the execution of finger movements. In spite of these findings regarding the control of force, little is known about the relation between force control and timing in the performance of bimanual tasks. In a series of studies, Keele and colleagues (Keele & Ivry, 1987; Keele, Ivry, & Pokorny, 1987; Keele, Pokorny, Corcos, & Ivry, 1985) examined the relation between timing and force control in unimanual movements, and culminated evidence for separate computational modules for timing and force control. For example, Keele et al. (1987) reported that the accuracy of the controlling muscle force was uncorrelated with the precision of timing control during repeated isometric force production, and concluded that force control was largely independent of timing in this task. However, Billon and Semjen and colleagues reported marked interactions between the two parameters during the unimanual production of periodic fingertapping sequences (Billon & Semjen, 1995; Billon, Semjen, & Stelmach, 1996), as well as during the production of short tapping sequences of six taps with a single accentuated tap (Semjen & Garcia-Colera, 1986; Semjen, Garcia-Colera, & Requin, 1984). In earlier work, which was done from the viewpoint of information processing, they hypothesized that an intrinsically variable (‘‘noisy’’) clock triggers tapping movements via intrinsically variable motor delays, resulting in intrinsically variable intertap intervals (ITIs). In later studies, however, they found that the ITIs were less variable than the initiation of the downward movement in the trajectory, suggesting that the endpoint rather than the onset is programmed. Sternad, Dean, and Newell (2000) also pointed out that timing and force control are tightly intertwined in both paced and self-paced rhythmic tapping tasks. Although the mean force was independent of the mean ITI, interdependency was observed in the variability estimates. Inui and Ichihara (2001) further examined the relation between timing and force control during finger-tapping sequences performed by both pianists and nonpianists. Their data suggested that participants switched from separate, parallel control of time and force in slow and moderate movements to a form of integrated, coupled control in fast movements. The ratios of time-to-peak force to press duration increased linearly in pianists but varied irregularly in nonpianists as the required force level increased. Pianists regulate peak force by timing the control of peak force to press duration, suggesting that training affects the relationship between these two parameters. As stated, during bimanual force production the dominant hand produces more force than the nondominant hand. This inherent asymmetry suggests that the control of timing may be more tightly coupled in the motor system than the control of force. In the present study, we examined this hypothesis of asymmetric control of force and symmetric control of timing in the bimanual production of finger-tapping tapping sequences. In so doing, we extend and capitalize on our previous work on unimanual tapping (Inui & Ichihara, 2001), following essentially the same method of analysis. Relative to the existing literature, the uniqueness of the present protocol was that
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temporal measures were analyzed in addition to the more extensively used kinetic measures in the study of fine-force control (Henningsen et al., 1995; Henningsen, Knecht, & Ende-Henningsen, 1997).
2. Methods 2.1. Participants Ten healthy right-handed male undergraduate students participated in the experiment. Their ages ranged from 20 to 23 years, with a mean of 21.8. Handedness was tested using a Japanese version of the Edinburgh handedness inventory (Oldfield, 1971). Informed consent for participation in the experiment was obtained from all participants. 2.2. Apparatus The participants were instructed to tap on two load cells (LUB-5KB, KYOWA, rated load: 5 kg), with a nonlinearity of 0.01% rated output and a hysteresis of 0.01% or 0.02% rated output (Fig. 1). The output of the load cells was amplified by a strain amplifier (MCC-8A, KYOWA) and displayed on an oscilloscope (MD625BM-12, Leader), so that the participant could see the difference between the peak forces produced and the target force, which was indicated on the oscilloscope by a single horizontal line. The force output was also recorded by a personal computer (Macintosh G3, Apple) and monitored on a screen (RD17V, Mitsubishi, 832 624 pixel resolution) after the amplified signal was converted from analogue to digital (Mac Lab MKIII, AD Instruments).
Fig. 1. Experimental setup.
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2.3. Measurements During a trial, 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. 2A shows a data sample. ITI, peak force, press duration, and time-to-peak force were measured automatically during each trial. These parameters are defined schematically in Fig. 2B. The ITI was defined as the onset-to-onset times of the tap. The force of each tap was defined as the peak output voltage from the load cell. Press duration was defined as the time that the participant’s finger was in contact with the load cell. Time-to-peak force was defined as the time to reach peak force. In addition to these parameters, the ratio of time-to-peak force to duration of press was calculated to examine the relationship between the timing of the peak force and press duration.
2.4. Procedure Participants performed both unimanual and bimanual finger-tapping tasks, which consisted of producing a target force of 200 g at a prescribed ITI of 400 ms. (These values were chosen on the basis of a previous study (Inui, Ichihara, Minami, & Matsui, 1998) in which the preferred mean peak force and mean ITI approximated these values.) In the unimanual tasks, the participants were instructed to match the target force at a prescribed ITI with either the right or the left hand, whereas in the bimanual tasks they had to match the target force and the prescribed ITI with both hands simultaneously. In the practice trials of the unimanual task, visual feedback was provided of the force output of the tapping hand. In the practice trials of the bimanual task, unilateral visual feedback was provided of the force output of either the dominant or the nondominant hand. The participants were seated facing the load cell (see Fig. 1) with their hand palms resting on a 6 cm high support. From this posture, they produced tapping movements by means of a slight extension–flexion pulse of the index finger at the metacarpophalangeal joint. Tapping rate was prescribed by means of a computer-controlled auditory metronome. Participants were instructed to synchronize their finger taps on the load cell with the metronome. A horizontal line on the oscilloscope indicated the target force of 200 g. Each participant tapped for 30 s in three practice trials. These trials served to acquaint the participant with the tapping task. While the participants attempted to synchronize their taps with the tones in the practice trials, they proceeded to produce the target force. If the participants were unable to produce the three consecutive practice trials with an average deviation from the target force of 10% or less and a within-trial coefficient of variation of the force produced of 30% or less, then practice trials were repeated two or three times. However, participants were not allowed to perform more than three additional trials to avoid fatigue of the hands and fingers. Two subjects failed to meet the criteria on the practice trials. On the recall trials immediately after the completion of the practice trials, each participant tapped once for 30 s. The participants were instructed to recall the force and the ITI as acquired during practice by means
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Fig. 2. Data sample (A) and the definition and measurement of the dependent variables (B). The data under conditions for required ITI 400 ms and force 200 g were sampled and digitized by an A/D converter after amplification and filtering.
of self-pacing without feedback. If the participants were unable to accurately produce the force according to the aforementioned criteria with regard to the average
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deviations and within-trial CVs in the practice trials, then the recall trial was conducted once again after practice trials were repeated two or three times. 2.5. Statistical analysis The dependent measures focused upon in the analysis of the recall trials were the means of ITI, peak force, and ratio of time-to-peak force to duration of press produced. The means were calculated over 30 measures in each trial as produced by each participant. To justify the use of the CV for both ITI and peak force, Pearson correlations were calculated between the standard deviation and the mean of both measures in each condition. There were 3 (task) 2 (effector: right vs. left hand) 2 (measure: peak force and ITI) conditions. The 12 coefficients of correlation ranged between 0.199 and 0.551 (df ¼ 8, ns). Because there was a similarly sloped linear relationship between the standard deviation and the mean for both measures, the use of the CV in comparing their variability was deemed justified. A 3 (task) 2 (effector) factorial ANOVA was performed to examine the effects of task and effector on the individual means of the dependent variables. The tapping movements as performed by the left and the right hand in the unimanual tasks were treated as a single level under the factor task. The other two levels under this factor were the two bimanual tasks with feedback of the force output of either the right or left hand. A 3 (task) 2 (effector) 2 (measure) factorial ANOVA was performed on the CVs of the dependent variables in order to be able to compare the variability of timing and force production across the experimental conditions.
3. Results Fig. 3 shows the group means of peak force (A) and ITI (B) in the recall trials of the three tasks. Although the ANOVA on peak force revealed no significant main effect of task, the peak force of the right hand was significantly larger than that of the left hand (F1;54 ¼ 16.02, p < 0:0005), in the absence of a significant interaction. The ANOVA on ITI yielded no significant effects. Mean ITIs were about 390 ms across all tasks, and the ITIs were consequently a little shorter on average than the target ITI. Thus, as compared to the force output, the ITIs were quite accurately controlled across all tasks. Fig. 3 also shows the group means of the CVs of peak force (C) and ITI (D) in the recall trials of the three tasks. The ANOVA revealed that the CVs of peak force were significantly larger than those of ITI (F1;108 ¼ 1019:98, p < 0:0001). In the unimanual tasks, the left hand had a larger CV for peak force than the right hand. In the bimanual tasks, although there was no significant difference between the CVs for the peak forces of both hands after feedback had been provided of the force output of the right hand, the right hand had a larger CV for peak force than the left hand after feedback had been given of the force output of the left hand. As a result, the task effector (F2;108 ¼ 28:06, p < 0:0001) and task effector measure interactions (F2;108 ¼ 16:02, p < 0:0001) were significant.
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Fig. 3. Means of peak force (A), ITI (B), and coefficients of variation of peak force (C) and ITI (D) under three conditions. The horizontal line as the target force and ITI in panels A and B indicates deviations from the targets. Abbreviations – Unimanual: the tapping movement of either the right or the left hand. Bimanual (RF): the tapping movement of both hands with visual feedback representing the force output of the right hand. Bimanual (LF): the tapping movement of both hands with visual feedback representing the force output of the left hand.
Fig. 4 shows the mean ratios of time-to-peak force to press duration in the recall trials of the three tasks. The ANOVA revealed that, although there was no significant difference between the ratios for the tasks, the ratios corresponding to the left hand were significantly larger than those corresponding to the right hand (F1;54 ¼ 4:51, p < 0:05). In other words, the ratio of interest increased as peak force decreased, which is consistent with our previous study (Inui & Ichihara, 2001). The task effector interaction was not significant.
4. Discussion 4.1. Asymmetric control of muscle force A main result of the present study was the observation of an asymmetry in force production: a larger force was exerted with the index finger of the dominant hand than with that of the nondominant hand in the bimanual tapping sequences. Henningsen et al. (1995) also found that the force output of the dominant hand was larger than that of the nondominant hand during the simultaneous matching of
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Fig. 4. Ratios of time-to-peak force to press duration (peak time/duration ratio) under three conditions. Abbreviations as in Fig. 4.
bilateral isometric finger flexion forces. Thus, the force output is influenced by the handedness of the subjects in both finger-tapping and isometric finger flexion tasks. During bimanual tapping, the motor outputs are commonly synchronized when constraints for independent action are absent. Considering that movements can be triggered by subliminal stimuli ðfor a review, see Gandevia (1996)Þ, the results of the present study suggest that the observed asymmetry may be due to anatomical or physiological asymmetries inherent to the motor system. For example, Nathan, Smith, and Deacon (1990) reported that the pyramidal tract is asymmetric in about 75% of the population. Because more fibers cross from the dominant hemisphere than from the nondominant, there are more fibers in the tract on the dominant side than on the nondominant side. This suggests that the primary motor cortex on the dominant side contains more pyramidal cells. Using cortical mapping studies in monkeys, Nudo, Jenkins, Merzenich, Prejean, and Grenda (1992) further showed that the dominant primary motor cortex has a larger area, higher spatial complexity, and a larger distal forelimb representation than the nondominant primary motor cortex. Furthermore, brain imaging studies reported motor cortical asymmetries during finger movements. Using positron emission tomography, Kawashima et al. (1993) found an increased regional blood flow in the dominant primary motor and premotor areas during movements of the dominant hand, suggesting that there is a differential increase in dominant and nondominant hemispheres when performing
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bimanual movements. Similarly, using functional magnetic resonance imaging, Kim et al. (1983) reported asymmetric activation patterns of the precentral gyri during the performance of repetitive finger movements. Thus, asymmetric activation in primary motor and premotor areas, as well as asymmetries in the corticospinal tract and a larger cortical hand representation on the dominant side, may elicit higher forces in the dominant hand. Using transcranial magnetic stimulation, Triggs, Calvaino, Macdonell, Cros, and Chiappa (1994) found that the threshold for activation of hand muscles is lower in the dominant than in the nondominant hemisphere. Henningsen et al. (1995) used this fact to explain the asymmetric production of muscle force in bimanual isometric tasks. However, some recent reports showed that motor excitability at rest is similar in the two hemispheres of right- and left-handed subjects (Brouwer, Sale, & Nordstrom, 2001; Semmler & Nordstrom, 1998; Triggs, Subramanium, & Rossi, 1999). These contradictory findings may be caused by methodological differences in the transcranial magnetic stimulation protocol. Because Triggs et al. (1994) used a circular coil positioned at the vertex for activation of either the left or right hemisphere, it may have been the case that they did not stimulate at the optimal side for evoking a response in the test muscle. Brouwer et al. (2001) concluded from this that resting excitability of motor cortex neurons activating the test muscle was equivalent in each hemisphere, and that threshold transcranial magnetic stimulation intensity produced descending corticospinal volleys of similar effectiveness on each side. Contrary to the suggestion of Henningsen et al. (1995), therefore, the asymmetric production of muscle force in bimanual tapping sequences cannot be explained by a lower threshold for activation of hand muscles as compared to the nondominant hemisphere. 4.2. Symmetric control of movement timing In the current study, no significant difference was found between the ITIs produced by the index fingers of both hands when performing the bimanual finger-tapping sequences. Keele and colleagues (Keele & Hawkins, 1982; Keele et al., 1987; Keele et al., 1985) accumulated evidence suggesting that the same central timekeeper controls different effectors during a task of repeated isometric force production or tapping sequences. For example, Keele and Hawkins (1982) found that the maximum rate in tapping sequences is correlated at 0.5 or more across such diverse effectors as finger, thumb, wrist, forearm, and foot. Keele et al. (1985) also reported that subjects who are regular at timing with one effector, such as the finger, also tend to be regular with another, such as the foot. They further observed a significant correlation between timing and perceptual acuity in a temporal judgment task. Using transcranial stimulation, Brouwer et al. (2001) examined the possibility that an asymmetry in the corticospinal activation of the two hands may be related to hand preference and interlimb differences in manual performance. They found that the asymmetry of facilitation of the muscle evoked potential was uncorrelated with differences between the hands in terms of finger-tapping speed or performance on a pegboard task, whereas it was associated with relative differences in the strength of the first dorsal interosseous. These findings are consistent with those obtained in the
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present study, which support the hypothesis of asymmetric control of force and symmetric control of movement timing in the context of a bimanual tapping task. 4.3. Neuroscientific bases of bimanual finger tapping It has been demonstrated that the activity of single neurons in the primary motor area of the cerebral cortex contain an encoding of force (Evarts, 1968; Hepp-Reymond, 1988). On the other hand, lateral cerebellar lesions can disrupt the timing of movement components in complex tasks, in that they are no longer smoothly coordinated but appear to be controlled sequentially (Holmes, 1939; Ivry, Keele, & Denier, 1988). Thus, whereas the primary motor cortex plays a prominent role in the control of muscle force of finger movements, the lateral cerebellum is probably involved in their timing. Based on the existing neuroscientific literature, we suggest that, although it is clearly an oversimplification, the scheme depicted in Fig. 5 provides an account
Fig. 5. The main neural connections playing a role in the production of bimanual movements. Two large filled circles show the pyramidal cells in the primary motor area of the cerebral cortex. To indicate that the pyramidal tract is asymmetric, while a thick descending arrow shows the tract on the dominant side, a thin descending arrow shows the tract on the nondominant side. Commissural fibers generally interconnect corresponding areas in the two hemispheres through the corpus callosum (two parallel dashed arrows). Two small filled circles represent the dentate nuclei in the lateral cerebellar hemisphere. The lateral cerebellum receives contralateral cerebral inputs via the pontine nuclei (two descending dashed arrows), and efferent fibers from the dentate nuclei project to the contralateral primary motor cortex via the thalamus (two ascending arrows). Abbreviations – Cbr: cerebral cortex; Cbl: lateral cerebellum.
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for the present findings. The two filled circles at the top of the figure represent the pyramidal cells in the primary motor cortex. To indicate that the pyramidal tract is asymmetric, the tract on the dominant side is represented by a thick descending and the tract on the nondominant side by a thin descending arrow. Commissural fibers generally interconnect corresponding areas in the two hemispheres through the corpus callosum, which is indicated by the two parallel horizontal dashed arrows. The two small filled circles in the middle of the figure represent the dentate nuclei in the lateral cerebelllar hemisphere. The lateral cerebellum receives contralateral cerebral inputs via the pontine nuclei, as is represented by the two descending dashed arrows, and efferent fibers from the dentate nuclei extensively project to the contralateral primary motor cortex via the thalamus, as is represented by the two crossing ascending arrows. Neuroanatomically, the cerebellar cortex is composed of three well-defined layers, which are uniformly structured (Brodal, 1998; Carpenter & Suttin, 1983). To date, no commissural fibers have been found. Thus, because neither a left–right difference nor an interaction between the cerebellar hemispheres is known, we assume that the same information pertaining to motor timing of each index finger may be transmitted from the dentate nucleus to the contralateral primary motor cortex. In the cerebrum, in contrast, although all parts of the neocortex consist of six cell layers, the thickness and structure of the layers vary from one area to the next. In addition, there is a vast number of commissural fibers running through the corpus callosum. Thus, there are marked left–right differences and substantial interactions between both hemispheres. Furthermore, the density of the commissural fibers varies across cortical regions. Whereas primary motor and somatosensory cortices corresponding to body parts that usually perform tasks independently of each other, such as the hands and the feet, possess few commissural fibers, cortices corresponding to body parts that usually perform in a symmetrical fashion, such as two halves of the back, are amply interconnected (Myers, 1965). Commissural connections between hand areas perhaps disturb the independent control of the hands. However, Brodal (1998) emphasized that via commissural connections of other cortical areas, information about motor commands and sensory signals pertaining to the distal body parts reach both hemispheres. Furthermore, in monkeys, clusters of neurons have been discovered in the primary motor cortex which correspond bilaterally to the distal hand muscles (Aizawa, Mushiake, Inase, & Tanji, 1990; Matsunami & Hamada, 1981). Thus, because there is little information about the movement commands of both the index fingers via few commissural fibers and bilateral corticospinal fibers, force of both the fingers may be loosely coupled by these fibers. Although not represented in Fig. 5, several studies have found that, in monkeys, a number of neurons in the supplementary motor area (Brinkman & Porter, 1979; Tanji, Okano, & Sato, 1988) and the premotor cortex (Gentilucci et al., 1988) are specifically engaged in the execution of bilateral movements. From clinical findings of premotor and supplementary motor lesions and ablation studies in monkeys, Wiesendanger, Wicki, and Rouiller (1994) argued that these cortical areas are responsible for temporal and spatial coupling of both hands when they are engaged
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in purposeful cooperative manipulations. For example, in rhythmic bilateral movements, reaching for heavy objects, and catching a ball, both hands or arms are often put into action simultaneously. This control of bilaterally synchronized initiation may be achieved by bilateral projections from the premotor and supplementary motor cortices to the spinal cord. These bilateral innervations would guarantee a tight coupling as a symmetrical control of timing was observed in the bimanual tapping movements in the present study. 4.4. Role of visual feedback In the present study, after practice with feedback pertaining to the force output of the nondominant hand, the CV of the peak force of the dominant hand was significantly larger than that of the nondominant hand. However, after practice with feedback pertaining to the force output of the dominant hand, the peak forces produced by the hands did not differ significantly. In contrast, in a bilateral isometric finger task, Henningsen et al. (1995) found that when unilateral feedback represented the force output of the dominant hand, the asymmetry, in which a larger force was exerted with the index finger of the dominant hand, was no longer present, whereas, when the feedback concerned the force output of the nondominant hand, the asymmetry was still observed. A possible explanation for this discrepancy in results could reside in the difference in experimental tasks. Whereas Henningsen et al. (1995) used an isometric task, we employed a tapping task. Since the speed of force production was not prescribed in their experiment whereas it was in ours, the participants of the present study took little time to produce a peak force. In the current study, therefore, although the results on mean force showed no influence of the feedback of the dominant hand, the influence is only observed in the variability estimates. The dominant hand has been demonstrated to be superior to the nondominant hand in tracking tasks involving visual feedback (Goodale, 1988). In a task requiring the simultaneous rotation of both hands at different angular velocities to trace a diagonal line, Fagard, Morioka, and Wolff (1985) also found that the dominant hand made fewer directional errors than the nondominant hand. Thus, like previous studies, the results of the present study suggest that the coupling to visual information is more efficient with the dominant than with the nondominant hand ðsee also Honda (1981)Þ.
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Asymmetric control of force and symmetric control of timing in bimanual finger tapping Nobuyuki Inui a
a,*
, Hiroshi Hatta
b
Department of Human Motor Control, Faculty of Health and Living Sciences, Naruto University of Education, Takashima, Naruto-cho, Naruto-shi 772-8502, Japan b Graduate School of Education, Naruto University of Education, Takashima, Naruto-cho, Naruto-shi 772-8502, Japan Accepted 27 March 2002
Abstract An experiment was conducted to examine the control of force and timing in bimanual finger tapping. Participants were trained to produce both unimanual (left or right hand) and bimanual finger-tapping sequences with a peak force of 200 g and an intertap interval (ITI) of 400 ms. During practice, visual force feedback was provided pertaining to the hand performing the unimanual tapping sequences and to either the dominant or the nondominant hand in the bimanual tapping sequences. After practice, the participants produced the learned unimanual and bimanual tapping sequences in the absence of feedback. In those trials the force produced by the dominant (right) hand was significantly larger than that produced by the nondominant (left) hand, in the absence of a significant difference between the ITIs produced by both hands. Furthermore, after unilateral feedback had been provided of the force produced by the nondominant hand, the force output of the dominant hand was significantly more variable than that of the nondominant hand. In contrast, after feedback had been provided of the force produced by the dominant hand, the variability of the force outputs of the two hands did not differ significantly. These results were discussed in the light of both neurophysiological and anatomical findings, and were interpreted to imply that the control of timing (in bimanual tasks) may be more tightly coupled in the motor system than the control of force. Ó 2002 Elsevier Science B.V. All rights reserved.
*
Corresponding author. Tel.: +81-088-684-6517; fax: +81-088-687-6028. E-mail address: [email protected] (N. Inui).
0167-9457/02/$ - see front matter Ó 2002 Elsevier Science B.V. All rights reserved. PII: S 0 1 6 7 - 9 4 5 7 ( 0 2 ) 0 0 0 9 4 - 5
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PsycINFO classification: 2330 Keywords: Force control; Movement timing; Bimanual tapping
1. Introduction In the last two decades, the coordination between bimanual rhythmic movements has been studied extensively in experiments using finger oscillations (Kelso, 1984), finger tapping (Yamanishi, Kawato, & Suzuki, 1980), wrist rotations (Carson, Byblow, & Goodman, 1994), and whole arm movements (Swinnen & Walter, 1991). Persistent and robust findings in this line of research have been that: (1) in-phase (simultaneous) and antiphase (alternating) movements are the only phase relations that are stable and easy to achieve without practice (Yamanishi et al., 1980); (2) in-phase movements are more stable than antiphase movements (Scholz & Kelso, 1990), and (3) the stability of in-phase and antiphase movements decreases with increasing movement frequency (Post, Peper, & Beek, 2000). However, these studies on bimanual rhythmic movements typically focus on kinematical measures only. To date, the ability to coordinate rhythmic bimanual movements with kinetic measures has seldom been studied ða notable exception is a recent study by Peper and Carson (1999)Þ. Nevertheless, it may be argued that, in order to develop a more complete understanding of bimanual coordination, it is essential to examine how both timing and force production of bimanual hand movements are controlled. Like timing and relative phasing, isometric force production has been studied extensively in bimanual tasks. Henry and Smith (1961) found that the maximal force that can be produced by each hand in a bimanual grip task is less than the maximal force that can be produced by each hand separately. This bilateral deficit was also reported using static flexion of the wrist (Kroll, 1965) and static extension of the leg (Secher, Rorsgaard, & Secher, 1978). Using a static grip and a static flexion and extension of the elbow, in combination with EMG recordings, Ohtsuki (1994) found that besides the bilateral deficit, the reaction time of simultaneous bimanual responses is longer than that of unimanual responses. To identify the mechanisms underlying the bilateral deficit, Taniguchi, Burle, Vidal, and Bonnet (2001) examined an electroencephalographic correlate of the bilateral deficit during the preparation and execution stages of a reaction-time task. They found that the activation of the sensorimotor area of the right hand directly involved in voluntary control is weaker for bilateral than for unilateral contralateral responses. On the basis of this finding, they hypothesized that a transcallosal inhibitory effect persists in the bilateral response. In young children, the intentional production of force in one hand is accompanied by the unintentional production of force in the other hand (Lazarus & Todor, 1987; Todor & Lazarus, 1986). Although the unintentionally produced force is much smaller than the intentionally produced force, the similarity in the patterns of force production evidences that the control of manual force output is coupled in the immature human motor system. Henningsen, Ende-Henningsen, and Gordon (1995) examined the ability of adults to match the voluntary isometric finger flexion forces of the
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dominant with those of the nondominant hand, and found that larger forces were exerted with the index finger of the dominant hand. This finding suggests the presence of asymmetrical hemispheric thresholds for hand muscle activation, as well as an asymmetrical regional blood flow in the primary motor and premotor areas during the execution of finger movements. In spite of these findings regarding the control of force, little is known about the relation between force control and timing in the performance of bimanual tasks. In a series of studies, Keele and colleagues (Keele & Ivry, 1987; Keele, Ivry, & Pokorny, 1987; Keele, Pokorny, Corcos, & Ivry, 1985) examined the relation between timing and force control in unimanual movements, and culminated evidence for separate computational modules for timing and force control. For example, Keele et al. (1987) reported that the accuracy of the controlling muscle force was uncorrelated with the precision of timing control during repeated isometric force production, and concluded that force control was largely independent of timing in this task. However, Billon and Semjen and colleagues reported marked interactions between the two parameters during the unimanual production of periodic fingertapping sequences (Billon & Semjen, 1995; Billon, Semjen, & Stelmach, 1996), as well as during the production of short tapping sequences of six taps with a single accentuated tap (Semjen & Garcia-Colera, 1986; Semjen, Garcia-Colera, & Requin, 1984). In earlier work, which was done from the viewpoint of information processing, they hypothesized that an intrinsically variable (‘‘noisy’’) clock triggers tapping movements via intrinsically variable motor delays, resulting in intrinsically variable intertap intervals (ITIs). In later studies, however, they found that the ITIs were less variable than the initiation of the downward movement in the trajectory, suggesting that the endpoint rather than the onset is programmed. Sternad, Dean, and Newell (2000) also pointed out that timing and force control are tightly intertwined in both paced and self-paced rhythmic tapping tasks. Although the mean force was independent of the mean ITI, interdependency was observed in the variability estimates. Inui and Ichihara (2001) further examined the relation between timing and force control during finger-tapping sequences performed by both pianists and nonpianists. Their data suggested that participants switched from separate, parallel control of time and force in slow and moderate movements to a form of integrated, coupled control in fast movements. The ratios of time-to-peak force to press duration increased linearly in pianists but varied irregularly in nonpianists as the required force level increased. Pianists regulate peak force by timing the control of peak force to press duration, suggesting that training affects the relationship between these two parameters. As stated, during bimanual force production the dominant hand produces more force than the nondominant hand. This inherent asymmetry suggests that the control of timing may be more tightly coupled in the motor system than the control of force. In the present study, we examined this hypothesis of asymmetric control of force and symmetric control of timing in the bimanual production of finger-tapping tapping sequences. In so doing, we extend and capitalize on our previous work on unimanual tapping (Inui & Ichihara, 2001), following essentially the same method of analysis. Relative to the existing literature, the uniqueness of the present protocol was that
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temporal measures were analyzed in addition to the more extensively used kinetic measures in the study of fine-force control (Henningsen et al., 1995; Henningsen, Knecht, & Ende-Henningsen, 1997).
2. Methods 2.1. Participants Ten healthy right-handed male undergraduate students participated in the experiment. Their ages ranged from 20 to 23 years, with a mean of 21.8. Handedness was tested using a Japanese version of the Edinburgh handedness inventory (Oldfield, 1971). Informed consent for participation in the experiment was obtained from all participants. 2.2. Apparatus The participants were instructed to tap on two load cells (LUB-5KB, KYOWA, rated load: 5 kg), with a nonlinearity of 0.01% rated output and a hysteresis of 0.01% or 0.02% rated output (Fig. 1). The output of the load cells was amplified by a strain amplifier (MCC-8A, KYOWA) and displayed on an oscilloscope (MD625BM-12, Leader), so that the participant could see the difference between the peak forces produced and the target force, which was indicated on the oscilloscope by a single horizontal line. The force output was also recorded by a personal computer (Macintosh G3, Apple) and monitored on a screen (RD17V, Mitsubishi, 832 624 pixel resolution) after the amplified signal was converted from analogue to digital (Mac Lab MKIII, AD Instruments).
Fig. 1. Experimental setup.
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2.3. Measurements During a trial, 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. 2A shows a data sample. ITI, peak force, press duration, and time-to-peak force were measured automatically during each trial. These parameters are defined schematically in Fig. 2B. The ITI was defined as the onset-to-onset times of the tap. The force of each tap was defined as the peak output voltage from the load cell. Press duration was defined as the time that the participant’s finger was in contact with the load cell. Time-to-peak force was defined as the time to reach peak force. In addition to these parameters, the ratio of time-to-peak force to duration of press was calculated to examine the relationship between the timing of the peak force and press duration.
2.4. Procedure Participants performed both unimanual and bimanual finger-tapping tasks, which consisted of producing a target force of 200 g at a prescribed ITI of 400 ms. (These values were chosen on the basis of a previous study (Inui, Ichihara, Minami, & Matsui, 1998) in which the preferred mean peak force and mean ITI approximated these values.) In the unimanual tasks, the participants were instructed to match the target force at a prescribed ITI with either the right or the left hand, whereas in the bimanual tasks they had to match the target force and the prescribed ITI with both hands simultaneously. In the practice trials of the unimanual task, visual feedback was provided of the force output of the tapping hand. In the practice trials of the bimanual task, unilateral visual feedback was provided of the force output of either the dominant or the nondominant hand. The participants were seated facing the load cell (see Fig. 1) with their hand palms resting on a 6 cm high support. From this posture, they produced tapping movements by means of a slight extension–flexion pulse of the index finger at the metacarpophalangeal joint. Tapping rate was prescribed by means of a computer-controlled auditory metronome. Participants were instructed to synchronize their finger taps on the load cell with the metronome. A horizontal line on the oscilloscope indicated the target force of 200 g. Each participant tapped for 30 s in three practice trials. These trials served to acquaint the participant with the tapping task. While the participants attempted to synchronize their taps with the tones in the practice trials, they proceeded to produce the target force. If the participants were unable to produce the three consecutive practice trials with an average deviation from the target force of 10% or less and a within-trial coefficient of variation of the force produced of 30% or less, then practice trials were repeated two or three times. However, participants were not allowed to perform more than three additional trials to avoid fatigue of the hands and fingers. Two subjects failed to meet the criteria on the practice trials. On the recall trials immediately after the completion of the practice trials, each participant tapped once for 30 s. The participants were instructed to recall the force and the ITI as acquired during practice by means
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Fig. 2. Data sample (A) and the definition and measurement of the dependent variables (B). The data under conditions for required ITI 400 ms and force 200 g were sampled and digitized by an A/D converter after amplification and filtering.
of self-pacing without feedback. If the participants were unable to accurately produce the force according to the aforementioned criteria with regard to the average
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deviations and within-trial CVs in the practice trials, then the recall trial was conducted once again after practice trials were repeated two or three times. 2.5. Statistical analysis The dependent measures focused upon in the analysis of the recall trials were the means of ITI, peak force, and ratio of time-to-peak force to duration of press produced. The means were calculated over 30 measures in each trial as produced by each participant. To justify the use of the CV for both ITI and peak force, Pearson correlations were calculated between the standard deviation and the mean of both measures in each condition. There were 3 (task) 2 (effector: right vs. left hand) 2 (measure: peak force and ITI) conditions. The 12 coefficients of correlation ranged between 0.199 and 0.551 (df ¼ 8, ns). Because there was a similarly sloped linear relationship between the standard deviation and the mean for both measures, the use of the CV in comparing their variability was deemed justified. A 3 (task) 2 (effector) factorial ANOVA was performed to examine the effects of task and effector on the individual means of the dependent variables. The tapping movements as performed by the left and the right hand in the unimanual tasks were treated as a single level under the factor task. The other two levels under this factor were the two bimanual tasks with feedback of the force output of either the right or left hand. A 3 (task) 2 (effector) 2 (measure) factorial ANOVA was performed on the CVs of the dependent variables in order to be able to compare the variability of timing and force production across the experimental conditions.
3. Results Fig. 3 shows the group means of peak force (A) and ITI (B) in the recall trials of the three tasks. Although the ANOVA on peak force revealed no significant main effect of task, the peak force of the right hand was significantly larger than that of the left hand (F1;54 ¼ 16.02, p < 0:0005), in the absence of a significant interaction. The ANOVA on ITI yielded no significant effects. Mean ITIs were about 390 ms across all tasks, and the ITIs were consequently a little shorter on average than the target ITI. Thus, as compared to the force output, the ITIs were quite accurately controlled across all tasks. Fig. 3 also shows the group means of the CVs of peak force (C) and ITI (D) in the recall trials of the three tasks. The ANOVA revealed that the CVs of peak force were significantly larger than those of ITI (F1;108 ¼ 1019:98, p < 0:0001). In the unimanual tasks, the left hand had a larger CV for peak force than the right hand. In the bimanual tasks, although there was no significant difference between the CVs for the peak forces of both hands after feedback had been provided of the force output of the right hand, the right hand had a larger CV for peak force than the left hand after feedback had been given of the force output of the left hand. As a result, the task effector (F2;108 ¼ 28:06, p < 0:0001) and task effector measure interactions (F2;108 ¼ 16:02, p < 0:0001) were significant.
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Fig. 3. Means of peak force (A), ITI (B), and coefficients of variation of peak force (C) and ITI (D) under three conditions. The horizontal line as the target force and ITI in panels A and B indicates deviations from the targets. Abbreviations – Unimanual: the tapping movement of either the right or the left hand. Bimanual (RF): the tapping movement of both hands with visual feedback representing the force output of the right hand. Bimanual (LF): the tapping movement of both hands with visual feedback representing the force output of the left hand.
Fig. 4 shows the mean ratios of time-to-peak force to press duration in the recall trials of the three tasks. The ANOVA revealed that, although there was no significant difference between the ratios for the tasks, the ratios corresponding to the left hand were significantly larger than those corresponding to the right hand (F1;54 ¼ 4:51, p < 0:05). In other words, the ratio of interest increased as peak force decreased, which is consistent with our previous study (Inui & Ichihara, 2001). The task effector interaction was not significant.
4. Discussion 4.1. Asymmetric control of muscle force A main result of the present study was the observation of an asymmetry in force production: a larger force was exerted with the index finger of the dominant hand than with that of the nondominant hand in the bimanual tapping sequences. Henningsen et al. (1995) also found that the force output of the dominant hand was larger than that of the nondominant hand during the simultaneous matching of
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Fig. 4. Ratios of time-to-peak force to press duration (peak time/duration ratio) under three conditions. Abbreviations as in Fig. 4.
bilateral isometric finger flexion forces. Thus, the force output is influenced by the handedness of the subjects in both finger-tapping and isometric finger flexion tasks. During bimanual tapping, the motor outputs are commonly synchronized when constraints for independent action are absent. Considering that movements can be triggered by subliminal stimuli ðfor a review, see Gandevia (1996)Þ, the results of the present study suggest that the observed asymmetry may be due to anatomical or physiological asymmetries inherent to the motor system. For example, Nathan, Smith, and Deacon (1990) reported that the pyramidal tract is asymmetric in about 75% of the population. Because more fibers cross from the dominant hemisphere than from the nondominant, there are more fibers in the tract on the dominant side than on the nondominant side. This suggests that the primary motor cortex on the dominant side contains more pyramidal cells. Using cortical mapping studies in monkeys, Nudo, Jenkins, Merzenich, Prejean, and Grenda (1992) further showed that the dominant primary motor cortex has a larger area, higher spatial complexity, and a larger distal forelimb representation than the nondominant primary motor cortex. Furthermore, brain imaging studies reported motor cortical asymmetries during finger movements. Using positron emission tomography, Kawashima et al. (1993) found an increased regional blood flow in the dominant primary motor and premotor areas during movements of the dominant hand, suggesting that there is a differential increase in dominant and nondominant hemispheres when performing
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bimanual movements. Similarly, using functional magnetic resonance imaging, Kim et al. (1983) reported asymmetric activation patterns of the precentral gyri during the performance of repetitive finger movements. Thus, asymmetric activation in primary motor and premotor areas, as well as asymmetries in the corticospinal tract and a larger cortical hand representation on the dominant side, may elicit higher forces in the dominant hand. Using transcranial magnetic stimulation, Triggs, Calvaino, Macdonell, Cros, and Chiappa (1994) found that the threshold for activation of hand muscles is lower in the dominant than in the nondominant hemisphere. Henningsen et al. (1995) used this fact to explain the asymmetric production of muscle force in bimanual isometric tasks. However, some recent reports showed that motor excitability at rest is similar in the two hemispheres of right- and left-handed subjects (Brouwer, Sale, & Nordstrom, 2001; Semmler & Nordstrom, 1998; Triggs, Subramanium, & Rossi, 1999). These contradictory findings may be caused by methodological differences in the transcranial magnetic stimulation protocol. Because Triggs et al. (1994) used a circular coil positioned at the vertex for activation of either the left or right hemisphere, it may have been the case that they did not stimulate at the optimal side for evoking a response in the test muscle. Brouwer et al. (2001) concluded from this that resting excitability of motor cortex neurons activating the test muscle was equivalent in each hemisphere, and that threshold transcranial magnetic stimulation intensity produced descending corticospinal volleys of similar effectiveness on each side. Contrary to the suggestion of Henningsen et al. (1995), therefore, the asymmetric production of muscle force in bimanual tapping sequences cannot be explained by a lower threshold for activation of hand muscles as compared to the nondominant hemisphere. 4.2. Symmetric control of movement timing In the current study, no significant difference was found between the ITIs produced by the index fingers of both hands when performing the bimanual finger-tapping sequences. Keele and colleagues (Keele & Hawkins, 1982; Keele et al., 1987; Keele et al., 1985) accumulated evidence suggesting that the same central timekeeper controls different effectors during a task of repeated isometric force production or tapping sequences. For example, Keele and Hawkins (1982) found that the maximum rate in tapping sequences is correlated at 0.5 or more across such diverse effectors as finger, thumb, wrist, forearm, and foot. Keele et al. (1985) also reported that subjects who are regular at timing with one effector, such as the finger, also tend to be regular with another, such as the foot. They further observed a significant correlation between timing and perceptual acuity in a temporal judgment task. Using transcranial stimulation, Brouwer et al. (2001) examined the possibility that an asymmetry in the corticospinal activation of the two hands may be related to hand preference and interlimb differences in manual performance. They found that the asymmetry of facilitation of the muscle evoked potential was uncorrelated with differences between the hands in terms of finger-tapping speed or performance on a pegboard task, whereas it was associated with relative differences in the strength of the first dorsal interosseous. These findings are consistent with those obtained in the
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present study, which support the hypothesis of asymmetric control of force and symmetric control of movement timing in the context of a bimanual tapping task. 4.3. Neuroscientific bases of bimanual finger tapping It has been demonstrated that the activity of single neurons in the primary motor area of the cerebral cortex contain an encoding of force (Evarts, 1968; Hepp-Reymond, 1988). On the other hand, lateral cerebellar lesions can disrupt the timing of movement components in complex tasks, in that they are no longer smoothly coordinated but appear to be controlled sequentially (Holmes, 1939; Ivry, Keele, & Denier, 1988). Thus, whereas the primary motor cortex plays a prominent role in the control of muscle force of finger movements, the lateral cerebellum is probably involved in their timing. Based on the existing neuroscientific literature, we suggest that, although it is clearly an oversimplification, the scheme depicted in Fig. 5 provides an account
Fig. 5. The main neural connections playing a role in the production of bimanual movements. Two large filled circles show the pyramidal cells in the primary motor area of the cerebral cortex. To indicate that the pyramidal tract is asymmetric, while a thick descending arrow shows the tract on the dominant side, a thin descending arrow shows the tract on the nondominant side. Commissural fibers generally interconnect corresponding areas in the two hemispheres through the corpus callosum (two parallel dashed arrows). Two small filled circles represent the dentate nuclei in the lateral cerebellar hemisphere. The lateral cerebellum receives contralateral cerebral inputs via the pontine nuclei (two descending dashed arrows), and efferent fibers from the dentate nuclei project to the contralateral primary motor cortex via the thalamus (two ascending arrows). Abbreviations – Cbr: cerebral cortex; Cbl: lateral cerebellum.
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for the present findings. The two filled circles at the top of the figure represent the pyramidal cells in the primary motor cortex. To indicate that the pyramidal tract is asymmetric, the tract on the dominant side is represented by a thick descending and the tract on the nondominant side by a thin descending arrow. Commissural fibers generally interconnect corresponding areas in the two hemispheres through the corpus callosum, which is indicated by the two parallel horizontal dashed arrows. The two small filled circles in the middle of the figure represent the dentate nuclei in the lateral cerebelllar hemisphere. The lateral cerebellum receives contralateral cerebral inputs via the pontine nuclei, as is represented by the two descending dashed arrows, and efferent fibers from the dentate nuclei extensively project to the contralateral primary motor cortex via the thalamus, as is represented by the two crossing ascending arrows. Neuroanatomically, the cerebellar cortex is composed of three well-defined layers, which are uniformly structured (Brodal, 1998; Carpenter & Suttin, 1983). To date, no commissural fibers have been found. Thus, because neither a left–right difference nor an interaction between the cerebellar hemispheres is known, we assume that the same information pertaining to motor timing of each index finger may be transmitted from the dentate nucleus to the contralateral primary motor cortex. In the cerebrum, in contrast, although all parts of the neocortex consist of six cell layers, the thickness and structure of the layers vary from one area to the next. In addition, there is a vast number of commissural fibers running through the corpus callosum. Thus, there are marked left–right differences and substantial interactions between both hemispheres. Furthermore, the density of the commissural fibers varies across cortical regions. Whereas primary motor and somatosensory cortices corresponding to body parts that usually perform tasks independently of each other, such as the hands and the feet, possess few commissural fibers, cortices corresponding to body parts that usually perform in a symmetrical fashion, such as two halves of the back, are amply interconnected (Myers, 1965). Commissural connections between hand areas perhaps disturb the independent control of the hands. However, Brodal (1998) emphasized that via commissural connections of other cortical areas, information about motor commands and sensory signals pertaining to the distal body parts reach both hemispheres. Furthermore, in monkeys, clusters of neurons have been discovered in the primary motor cortex which correspond bilaterally to the distal hand muscles (Aizawa, Mushiake, Inase, & Tanji, 1990; Matsunami & Hamada, 1981). Thus, because there is little information about the movement commands of both the index fingers via few commissural fibers and bilateral corticospinal fibers, force of both the fingers may be loosely coupled by these fibers. Although not represented in Fig. 5, several studies have found that, in monkeys, a number of neurons in the supplementary motor area (Brinkman & Porter, 1979; Tanji, Okano, & Sato, 1988) and the premotor cortex (Gentilucci et al., 1988) are specifically engaged in the execution of bilateral movements. From clinical findings of premotor and supplementary motor lesions and ablation studies in monkeys, Wiesendanger, Wicki, and Rouiller (1994) argued that these cortical areas are responsible for temporal and spatial coupling of both hands when they are engaged
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in purposeful cooperative manipulations. For example, in rhythmic bilateral movements, reaching for heavy objects, and catching a ball, both hands or arms are often put into action simultaneously. This control of bilaterally synchronized initiation may be achieved by bilateral projections from the premotor and supplementary motor cortices to the spinal cord. These bilateral innervations would guarantee a tight coupling as a symmetrical control of timing was observed in the bimanual tapping movements in the present study. 4.4. Role of visual feedback In the present study, after practice with feedback pertaining to the force output of the nondominant hand, the CV of the peak force of the dominant hand was significantly larger than that of the nondominant hand. However, after practice with feedback pertaining to the force output of the dominant hand, the peak forces produced by the hands did not differ significantly. In contrast, in a bilateral isometric finger task, Henningsen et al. (1995) found that when unilateral feedback represented the force output of the dominant hand, the asymmetry, in which a larger force was exerted with the index finger of the dominant hand, was no longer present, whereas, when the feedback concerned the force output of the nondominant hand, the asymmetry was still observed. A possible explanation for this discrepancy in results could reside in the difference in experimental tasks. Whereas Henningsen et al. (1995) used an isometric task, we employed a tapping task. Since the speed of force production was not prescribed in their experiment whereas it was in ours, the participants of the present study took little time to produce a peak force. In the current study, therefore, although the results on mean force showed no influence of the feedback of the dominant hand, the influence is only observed in the variability estimates. The dominant hand has been demonstrated to be superior to the nondominant hand in tracking tasks involving visual feedback (Goodale, 1988). In a task requiring the simultaneous rotation of both hands at different angular velocities to trace a diagonal line, Fagard, Morioka, and Wolff (1985) also found that the dominant hand made fewer directional errors than the nondominant hand. Thus, like previous studies, the results of the present study suggest that the coupling to visual information is more efficient with the dominant than with the nondominant hand ðsee also Honda (1981)Þ.
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