Limitations on coupling of bimanual movements caused by arm dominance: when the muscle homology principle fails.

Studies of bimanual movements typically report interference between motions of the two arms and preference to perform mirror-symmetrical patterns. However, recent studies have demonstrated that the two arms differ in the ability to control interaction torque (INT). This predicts limitations in the capability to perform mirror-symmetrical movements. Here, two experiments were performed to test this prediction. The first experiment included bimanual symmetrical and asymmetrical circle drawing at two frequency levels. Unimanual circle drawing was also recorded. The increases in cycling frequency caused differences between the two arms in movement trajectories in both bimanual modes, although the differences were more pronounced in the asymmetrical compared with the symmetrical mode. Based on torque analysis, the differences were attributed to the nondominant arm's decreased capability to control INT. The intraarm differences during the symmetrical pattern of bimanual movements were similar (although more pronounced) to those during unimanual movements. This finding was verified in the second experiment for symmetrical bimanual oval drawing. Four oval orientations were used to provide variations in INT. Similar to the first experiment, increases in cycling frequency caused spontaneous deviations from perfect bimanual symmetry associated with inefficient INT control in the nondominant arm. This finding supports the limitations in performing mirror-symmetrical bimanual movements due to differences in joint control between the arms. Based on our results and previous research, we argue that bimanual interference occurs during specification of characteristics of required motion, whereas lower-level generation of muscle forces is independent between the arms. A hierarchical model of bimanual control is proposed.

[1]  W Spijkers,et al.  Temporal coordination of alternative and simultaneous aiming movements of constrained timing structure , 1994, Psychological research.

[2]  A Semjen,et al.  Spontaneous and intentional pattern switching in a multisegmental bimanual coordination task. , 1999, Motor control.

[3]  Will Spijkers,et al.  The time course of cross-talk during the simultaneous specification of bimanual movement amplitudes , 1998, Experimental Brain Research.

[4]  E A Franz,et al.  Spatial Coupling in the Coordination of Complex Actions , 1997, The Quarterly journal of experimental psychology. A, Human experimental psychology.

[5]  S. Swinnen,et al.  Proprioceptive control of cyclical bimanual forearm movements across different movement frequencies as revealed by means of tendon vibration , 2001, Experimental Brain Research.

[6]  Roland R. Lee,et al.  Hemispheric asymmetries for kinematic and positional aspects of reaching. , 2004, Brain : a journal of neurology.

[7]  Nicole Wenderoth,et al.  Changes in Brain Activation during the Acquisition of a Multifrequency Bimanual Coordination Task: From the Cognitive Stage to Advanced Levels of Automaticity , 2005, The Journal of Neuroscience.

[8]  Nicole Wenderoth,et al.  Parieto-premotor areas mediate directional interference during bimanual movements. , 2004, Cerebral cortex.

[9]  J. Temprado,et al.  Effects of force production and trial duration on bimanual performance and attentional demands in a rhythmic coordination task. , 2008, Motor control.

[10]  S. P. Swinnen,et al.  Relative phase destabilization during interlimb coordination: the disruptive role of kinesthetic afferences induced by passive movement , 1990, Experimental Brain Research.

[11]  D. Wolpert,et al.  Simultaneous bimanual dynamics are learned without interference , 2007, Experimental Brain Research.

[12]  Daniel Cattaert,et al.  Hand coordination in bimanual circle drawing. , 1995 .

[13]  Robert L Sainburg,et al.  Shared bimanual tasks elicit bimanual reflexes during movement. , 2009, Journal of neurophysiology.

[14]  D. Sherwood Distance and location assimilation effects in rapid bimanual movement. , 1991, Research quarterly for exercise and sport.

[15]  S. P. Swinnen,et al.  Hierarchical control of different elbow-wrist coordination patterns , 1998, Experimental Brain Research.

[16]  Peter J. Beek,et al.  Modeling rhythmic interlimb coordination: The roles of movement amplitude and time delays , 1999 .

[17]  J. Annett,et al.  The Control of Movement in the Preferred and Non-Preferred Hands* , 1979, The Quarterly journal of experimental psychology.

[18]  C. Brinkman Supplementary motor area of the monkey's cerebral cortex: short- and long-term deficits after unilateral ablation and the effects of subsequent callosal section , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[19]  R. Sainburg,et al.  Differences in control of limb dynamics during dominant and nondominant arm reaching. , 2000, Journal of neurophysiology.

[20]  S. Swinnen,et al.  Between-limb asynchronies during bimanual coordination: Effects of manual dominance and attentional cueing , 1996, Neuropsychologia.

[21]  M. Laurent,et al.  Shared dynamics of attentional cost and pattern stability. , 2001, Human movement science.

[22]  Robert L Sainburg,et al.  Nondominant arm advantages in load compensation during rapid elbow joint movements. , 2003, Journal of neurophysiology.

[23]  S. Swinnen,et al.  Coordination of complex bimanual multijoint movements under increasing cycling frequencies: the prevalence of mirror-image and translational symmetry. , 2009, Acta psychologica.

[24]  M. Honda,et al.  Suppression of the non-dominant motor cortex during bimanual symmetric finger movement: A functional magnetic resonance imaging study , 2006, Neuroscience.

[25]  Richard G. Carson,et al.  The dynamics of isometric bimanual coordination , 1990, Experimental Brain Research.

[26]  Peter S. Lum,et al.  Greater reliance on impedance control in the nondominant arm compared with the dominant arm when adapting to a novel dynamic environment , 2007, Experimental Brain Research.

[27]  P. Brown,et al.  The importance of the dominant hemisphere in the organization of bimanual movements , 2003, Human brain mapping.

[28]  G. E. Stelmach,et al.  Commonalities and differences in control of various drawing movements , 2002, Experimental Brain Research.

[29]  D A Rosenbaum,et al.  Production of polyrhythms. , 1993, Journal of experimental psychology. Human perception and performance.

[30]  R. Sainburg Evidence for a dynamic-dominance hypothesis of handedness , 2001, Experimental Brain Research.

[31]  D. Brunt,et al.  Effects of tendon vibration on unimanual and bimanual movement accuracy , 1986, Experimental Neurology.

[32]  Natalia V Dounskaia,et al.  Influence of biomechanical constraints on horizontal arm movements. , 2002, Motor control.

[33]  M. Peters,et al.  Handedness: coordination of within- and between-hand alternating movements. , 1981, The American journal of psychology.

[34]  M T Turvey,et al.  Dynamical aspects of learning an interlimb rhythmic movement pattern. , 1992, Journal of motor behavior.

[35]  W. Prinz,et al.  Perceptual basis of bimanual coordination , 2001, Nature.

[36]  J. Diedrichsen Optimal Task-Dependent Changes of Bimanual Feedback Control and Adaptation , 2007, Current Biology.

[37]  Stephan P Swinnen,et al.  Exploring interlimb constraints during bimanual graphic performance: effects of muscle grouping and direction , 1998, Behavioural Brain Research.

[38]  Robert L Sainburg,et al.  Handedness: dominant arm advantages in control of limb dynamics. , 2002, Journal of neurophysiology.

[39]  Herbert Heuer,et al.  Control of the dominant and nondominant hand: exploitation and taming of nonmuscular forces , 2007, Experimental Brain Research.

[40]  Natalia Dounskaia,et al.  Egocentric and Allocentric Constraints in the Expression of Patterns of Interlimb Coordination , 1997, Journal of Cognitive Neuroscience.

[41]  J. Kelso Phase transitions and critical behavior in human bimanual coordination. , 1984, The American journal of physiology.

[42]  D Goodman,et al.  On the nature of human interlimb coordination. , 1979, Science.

[43]  Stephan P Swinnen,et al.  Asymmetric interlimb interference during the performance of a dynamic bimanual task , 1990, Brain and Cognition.

[44]  J. Summers,et al.  The Dynamics of Bimanual Circle Drawing , 1997, The Quarterly journal of experimental psychology. A, Human experimental psychology.

[45]  K. Mardia Statistics of Directional Data , 1972 .

[46]  S. P. Swinnen,et al.  Relative Phase Alterations During Bimanual Skill Acquisition. , 1995, Journal of motor behavior.

[47]  Robert L. Sainburg,et al.  Handedness: Differential Specializations for Control of Trajectory and Position , 2005, Exercise and sport sciences reviews.

[48]  C. MacKenzie,et al.  10 A Preliminary Theory of Two-Hand Cd-Ordinated Control , 1980 .

[49]  S. P. Swinnen,et al.  Generation of Bimanual Trajectories of Disparate Eccentricity: Levels of Interference and Spontaneous Changes Over Practice , 2002, Journal of motor behavior.

[50]  S. Swinnen Intermanual coordination: From behavioural principles to neural-network interactions , 2002, Nature Reviews Neuroscience.

[51]  C. B. Walter,et al.  The coordination of limb movements with different kinematic patterns , 1988, Brain and Cognition.

[52]  Andras Semjen,et al.  Instabilities during antiphase bimanual movements: are ipsilateral pathways involved? , 2003, Experimental Brain Research.

[53]  D. Anton Occupational biomechanics , 1986 .

[54]  P G Zanone,et al.  Evolution of behavioral attractors with learning: nonequilibrium phase transitions. , 1992, Journal of experimental psychology. Human perception and performance.

[55]  Natalia Dounskaia,et al.  Constraints during bimanual coordination: the role of direction in relation to amplitude and force requirements , 2001, Behavioural Brain Research.

[56]  Natalia Dounskaia,et al.  Efficient control of arm movements in advanced age , 2007, Experimental Brain Research.

[57]  D. Serrien Coordination constraints during bimanual versus unimanual performance conditions , 2008, Neuropsychologia.

[58]  Stephan P. Swinnen,et al.  Load compensation during homologous and non-homologous coordination , 1998, Experimental Brain Research.

[59]  V. Gurfinkel,et al.  Proprioceptive consequences of tendon vibration during movement. , 1995, Journal of neurophysiology.

[60]  Peter J. Beek,et al.  Frequency-induced phase transitions in bimanual tapping , 1995, Biological Cybernetics.

[61]  Natalia V Dounskaia,et al.  Directional biases reveal utilization of arm's biomechanical properties for optimization of motor behavior. , 2007, Journal of neurophysiology.

[62]  Nicole Wenderoth,et al.  Spatial interference during bimanual coordination: Differential brain networks associated with control of movement amplitude and direction , 2005, Human brain mapping.

[63]  D E Sherwood,et al.  Hand preference, practice order, and spatial assimilations in rapid bimanual movement. , 1994, Journal of motor behavior.

[64]  D J Ostry,et al.  Compensation for interaction torques during single- and multijoint limb movement. , 1999, Journal of neurophysiology.

[65]  Stephan P. Swinnen,et al.  Proprioceptive control of multijoint movement: bimanual circle drawing , 1999, Experimental Brain Research.

[66]  G. Koshland,et al.  Control of the wrist in three-joint arm movements to multiple directions in the horizontal plane. , 2000, Journal of neurophysiology.

[67]  C. MacKenzie,et al.  Bimanual Movement Control: Information processing and Interaction Effects , 1984 .

[68]  H N Zelaznik,et al.  Spatial topological constraints in a bimanual task. , 1991, Acta psychologica.