Elsevier

Neuroscience Research

Volume 163, February 2021, Pages 1-9
Neuroscience Research

Stability of bimanual finger tapping coordination is constrained by salient phases

https://doi.org/10.1016/j.neures.2020.02.007Get rights and content

Highlights

  • Tapping on the beat is stable in the order of the index, middle, and ring fingers.

  • Stability of bimanual four-finger tapping depends on that of unimanual tapping.

  • The relative-salience hypothesis can explain coordination of bimanual tapping.

Abstract

In bimanual cyclical continuous movements, the relative timing of the most salient movement phase in each movement is a predominant constraint. This is the case for coordination when both movements have a single most salient phase (the relative-salience hypothesis). We tested whether the relative-salience hypothesis could explain results obtained for repetitive discrete movements, utilizing finger tapping. In experiment 1, participants performed unimanual alternate two-finger tapping with the metronome beat (i.e., one finger taps on the beat and the other finger taps off the beat). The stability of the tapping timing relative to the beat, which reflects the extent of salience, was higher in the index finger than the middle finger, and was lower in the ring finger than the middle finger. In experiment 2, participants performed four conditions of repetitive bimanual four-finger tapping (i.e., alternate two-finger tapping in each hand) without external pacing signals. Under all four conditions, a more stable pattern occurred when the timing of the more salient tapping in each hand was simultaneous rather than alternate, regardless of relative direction in the external space or movement coupling of the homologous fingers. The results indicated that bimanual four-finger tapping could be explained by the relative-salience hypothesis.

Introduction

When performing cyclic joint movements bilaterally, there is a difference in movement stability depending on the relative direction of the movements in body based coordinates (Kelso, 1984; Swinnen, 2002). For example, when performing periodic abduction/adduction of both index fingers on the horizontal plane, the symmetrical pattern was more stable compared to the asymmetrical pattern (i.e., parallel) irrespective of the hand position (e.g., both hands were palm down, or one hand was palm down with the other hand was palm up) (Mechsner et al., 2001). That is, movement stability was independent of the coupling of muscle activations because symmetrical pattern was consisted by different couplings of muscle activation of two hands depending on the hand position. Superiority in movement stability of the symmetrical pattern compared to the asymmetrical pattern was observed in various bimanual coordinated movements using fingers (Kelso, 1984; Mechsner et al., 2001), wrists (Lee et al., 1996; Li et al., 2004), elbows (Kelso and Jeka, 1992; Serrien and Swinnen, 1999), and multi-joints (Mechsner et al., 2001; Serrien et al., 1999). Thus, Mechsner and his colleagues formulated the hypothesis that bimanual coordination can be explained by adopting a psychological viewpoint, that is, that bimanual coordination is organized to accomplish its perceptual goal such as a symmetrical pattern (Mechsner et al., 2001; Mechsner, 2004a, b).

Repetitive finger tapping movements have been used as an experimental paradigm to investigate various control mechanisms of bimanual coordination (Aoki et al., 2003; Aramaki et al., 2010; Yamanishi et al., 1979). Unlike the case of bimanual cyclical continuous movements, in which moving body parts did not touch anything at particular movement phases, repetitive bimanual four-finger tapping movements (i.e., alternate two-finger tapping in both left and right hands) with congruent or incongruent hand postures (e.g., both hands were palm down, or one hand was palm down with the other hand was palm up) revealed that co-activation of homologous muscles was more stable compared to co-activation of non-homologous muscles independent of the posture of the hands, that is, spatiotemporal symmetry of the tapping movement did not constrain bimanual tapping coordination (Riek and Woolley, 2005). At first glance, this neuromuscular constraint in bimanual repetitive discrete movements appears contrary to the above-mentioned interpretation of bimanual coordination by Mechsner.

Recently, we showed that movement stability in some kinds of bimanual coordination of cyclical continuous joint movements was predominantly constrained by a particular coupling of movements rather than by spatial symmetry (Zheng et al., 2018). For example, when performing periodic extension/flexion of the index finger bimanually, simultaneous flexion of the index finger was more stable compared to alternate flexion (e.g., flexion of the left index finger coupled with extension of the right index finger) irrespective of the spatial symmetry. The same is true of periodic pronation/supination of both forearms around a vertical axis. In these coordinated movements, each joint movement has a single most salient movement phase that surpasses the other movement phases. This supported the relative-salience hypothesis proposed by Mechsner (Mechsner, 2004a, b), which follows a perceptual grouping principle. What the relative-salience hypothesis means is as follows; when two cyclical bimanual movements are concurrently performed, if a “single” phase in each movement is perceptually conceived of as the most salient, then the salient phases of the two movements will have a strong tendency to go together. Otherwise, other perceptual goals such as spatiotemporal symmetry would be preferred in concurrent dual movements. A previous study showed that fingers were different from other body parts in motor function, and finger movement was related to motoric information in the internal world (Muraoka et al., 2015). It is still unclear whether the relative-salience hypothesis is able to explain the stability of the bimanual coordination using repetitive discrete movements such as bimanual finger tapping.

In the present study, we tested whether the relative-salience hypothesis could be extended to explain the stability relationships seen in bimanual four-finger tapping. In experiment 1, to test if there is a difference in the extent of salience among the tapping of different fingers, participants performed a sensorimotor coordination task. This involved the repeated, alternate tapping of two fingers in the same hand, synchronizing the tapping of one of two fingers with the beat of an auditory metronome (i.e., one finger taps on the beat and the other finger taps off the beat) (the rate of the beat: 1.5–3.5 Hz). The difference in the extent of salience was evaluated by the stability of synchronization. In experiment 2, based on the findings of experiment 1, we tested the relative-salience hypothesis by utilizing four kinds of bimanual four-finger tapping coordination patterns. Bimanual four-finger tapping coordination was performed without external auditory pacing signals in order to exclude the possibility that the bimanual coordination was produced by combining concurrent sensorimotor coordination in each hand between the pacing signal and finger movements. It is plausible that the tapping phase of each finger in the two finger alternate tapping pattern of one hand plays a similar role as the extreme joint positions in cyclical joint movements (e.g., the most extended or flexed position in cyclical finger extension/flexion) in terms of perception of salience in the movement. Thus, we hypothesized that the stability of bimanual repetitive discrete movements could also be explained by the relative-salience hypothesis, as with the case of bimanual cyclical continuous movements.

Section snippets

Participants

Twelve right handed participants (seven males and five females, mean age ± standard deviation: 25 ± 2 years) with no history of neuromuscular disorder or movement deficits volunteered to participate in this experiment. Before the experiment, all participants were fully informed about the purpose and procedure of the study, and signed a written consent form. The experimental procedure was approved by the Human Research Ethics Committee of Waseda University. The experiment was conducted in

Stability of unimanual two-finger tapping movement (experiment 1)

Phase transition times for each hand are shown in Fig. 2 for the right hand and in Fig. 3 for the left hand. The phase transition time was significantly greater for the I finger tapping on the beat as compared to the M finger tapping on the beat (right hand: t(11) = 3.31, corrected p = 0.02 [Fig. 2C]; left hand: t(11) = 3.80, corrected p = 0.01 [Fig. 3C]), and significantly greater for the M finger tapping on the beat as compared to the R finger tapping on the beat for both hands (right hand:

Discussion

The fundamental goal of this study was to examine whether the stability of bimanual repetitive discrete movements (i.e., bimanual four-finger tapping) could be explained by the relative-salience hypothesis. In experiment 1, we utilized unimanual alternate two-finger tapping of different finger combinations using the I, M, and R fingers. The tapping of one finger or the other was synchronized with the beat of an auditory metronome. The results showed that the degree of salience in finger tapping

Funding

This work was partly supported by JSPS KAKENHI Grant Number JP26350701.

Declaration of Competing Interest

None.

References (48)

  • R.G. Carson

    Neuromuscular-skeletal constraints upon the dynamics of perception-action coupling

    Exp. Brain Res.

    (1996)
  • R.G. Carson

    A simple and unified approach to human voluntary movements

    J Motor Behav.

    (2004)
  • R.G. Carson et al.

    Governing coordination: behavioural principles and neural correlates

    Exp. Brain Res.

    (2004)
  • R.G. Carson et al.

    Phase-transitions and critical fluctuations in rhythmic coordination of ipsilateral hand and foot

    J Motor Behav.

    (1995)
  • R.G. Carson et al.

    Artificial gravity reveals that economy of action determines the stability of sensorimotor coordination

    PLoS One

    (2009)
  • J. Duque et al.

    Monitoring coordination during bimanual movements: where is the mastermind?

    J. Cogn. Neurosci.

    (2009)
  • M. Fahrer

    Interdependent and independent actions of the fingers

  • C. Hager-Ross et al.

    Quantifying the independence of human finger movements: comparisons of digits, hands, and movement frequencies

    J. Neurosci.

    (2000)
  • C.M. Harris et al.

    Signal-dependent noise determines motor planning

    Nature

    (1998)
  • J.A. Kelso

    Phase transitions and critical behavior in human bimanual coordination

    Am. J. Physiol.

    (1984)
  • J.A. Kelso et al.

    Symmetry breaking dynamics of human multilimb coordination

    J. Exp. Psychol. Hum. Percept. Perform.

    (1992)
  • H. Kinoshita et al.

    Individual finger forces acting on a grasped object during shaking actions

    Ergonomics

    (1996)
  • A.J. Kovacs et al.

    Impossible is nothing: 5:3 and 4:3 multi-frequency bimanual coordination

    Exp. Brain Res.

    (2010)
  • K.S. Lashley

    The problem of serial order in behavior

  • View full text