A guide to performing difficult bimanual coordination tasks: just follow the yellow brick road

Both discrete and continuous bimanual coordination patterns are difficult to effectively perform when the two limbs are required to perform different movements patterns, move at different velocities and/or move different amplitudes unless some form of integrated feedback is provided. The purpose of the present experiment was to determine the degree to which a complex bimanual coordination pattern could be performed when integrated feedback and movement template are provided. The complex bimanual coordination pattern involved reciprocal movements of the two limbs under different difficulty requirements. As defined by Fitts’ index of difficulty (ID), the left arm (ID = 3, A = 16°, W = 4°) task was of lower difficulty than the right arm task (ID = 5, A = 32°, W = 2°). Note that the left and right limb movements are also different in terms of movement time, movement velocity, accuracy requirements and amplitude as well as one movement was continuous and the other intermittent. Participants were provided 2 blocks of 9 trials in the bimanual condition (30 s/trial). Following the bimanual phase, participants performed two unimanual test trials—one with each limb. The results demonstrated that the performance for each limb in the bimanual condition was similar to the performance for the same limb and conditions in the unimanual control conditions. The similarity was indicated by the same movement speed, movement structure, endpoint variability and hit rates for the bimanual and unimanual conditions. The results support our hypothesis that people can overcome the intrinsic difficulties associated with performing complex bimanual coordination patterns when provided appropriate perceptual information feedback that allows them to detect and correct coordination errors.     

Timing of bimanual movements and deafferentation: implications for the role of sensory movement effects

In a repetitive tapping task, the within-hand variability of intertap intervals is reduced when participants tap with both hands instead of single-handedly. This bimanual advantage has been attributed to timer as opposed to motor variance (according to the Wing-Kristofferson model; Helmuth and Ivry 1996) and related to the additional sensory consequences of the movement of the extra hand in the bimanual case (Drewing et al. 2002). In the present study the effect of sensory feedback of the movement on this advantage was investigated by comparing the results of a person (IW) deafferented below the neck with those of age-matched controls. IW showed an even more pronounced bimanual advantage than controls, suggesting that the bimanual advantage is not due to actual sensory feedback. These results support another hypothesis, namely that bimanual timing profits from the averaging of different central control signals that relate to each effectors movements.     

Bimanual and unimanual length perception

From previous studies, it is unclear how bimanual length discrimination differs from unimanual length discrimination. To investigate the difference, we designed an experiment with four conditions. In the first two conditions, unimanual and bimanual discrimination thresholds are determined. In the third and fourth conditions, length is explored with the two index fingers like in the bimanual condition, but the reference is either internal, by clasping the hands together, or external, by grasping handles connected to the table. We find that thresholds for the unimanual condition (7.0 %) and the clasping condition (9.2 %) are both lower than for the bimanual condition (16 %) and the grasping handles condition (15 %). We conclude that when discriminating length unimanually and bimanually while clasping the hands together, the internal reference within the hand can be used and that explains the lower discrimination thresholds     

The role of auditory and visual models in the production of bimanual tapping patterns

An experiment was designed to determine the effectiveness of auditory and visual models in the learning of a 2:3 bimanual tapping pattern. Participants were randomly assigned to an auditory model, visual model, auditory + visual model, or a control (visual metronome) group. The task for all groups was to tap a left side force transducer with the left hand and a right side force transducer with the right hand in attempt to produce the desired 2:3 bimanual coordination pattern. The auditory model consisted of a series of tones representing the goal pattern played prior to each practice trial. The visual model consisted of a visual display representing the goal tapping pattern. Visual pacing metronomes were provided to the control group. The right and left side metronomes flashed during the trial in a pattern representing the goal tapping pattern. Subjects in all groups performed 14 practice trials consisting of 15 s each devoted to tapping the goal pattern (total practice time = 3.5 min). A retention test without the aid of the models or metronomes was administered following the practice trials. The results for the model groups indicated extremely effective performance of the bimanual coordination patterns for the auditory, visual, and auditory + visual model conditions with not only the relative, but also the absolute characteristics of the models exhibited during retention testing. Retention performance for the visual metronome condition was less accurate and more variable than the three model conditions. In addition, the auditory + visual model condition resulted in retention performance that was more stable than the auditory model condition.     

Suppression of the non-dominant motor cortex during bimanual symmetric finger movement: a functional magnetic resonance imaging study

Patterns of bimanual coordination in which homologous muscles are simultaneously active are more stable than those in which homologous muscles are engaged in an alternating fashion. This may be attributable to the stronger involvement of the dominant motor cortex in ipsilateral hand movements via interaction with the non-dominant motor system, known as neural crosstalk. We used functional magnetic resonance imaging to investigate the neural representation of the interhemispheric interaction during bimanual mirror movements. Thirteen right-handed subjects completed four conditions: sequential finger tapping using the right and left index and middle fingers, bimanual mirror and parallel finger tapping. Auditory cues (3 Hz) were used to keep the tapping frequency constant. Task-related activation in the right primary motor cortex was significantly less prominent during mirror than unimanual left-handed movements. This was mirror- and non-dominant side-specific; parallel movements did not cause such a reduction, and the left primary motor cortex showed no such differential activation across the unimanual right, bimanual mirror, and bimanual parallel conditions. Reducing the contralateral innervation of the left hand may increase the fraction of the force command to the left hand coming from the left primary motor cortex, enhancing the neural crosstalk.     

Unimanual and bimanual voluntary movement in Huntington's disease

Unimanual and bimanual cyclical forearm movements were studied in 15 Huntington's disease (HD) patients and 15 healthy, gender- and age-matched controls. Whereas the unimanual task was only performed at maximal speed, the bimanual movements were performed according to the in-phase and anti-phase mode at different cycling frequencies. The HD patients also performed the tasks after 12 months of follow-up. Findings revealed that maximal cycling frequency during unimanual movement was significantly lower in HD patients as compared with controls. In addition, measures of relative phasing established that bimanual cyclical movements were performed with lower accuracy and higher variability in HD patients. The differential variability between both groups was magnified by increasing the cycling frequency and coordinative complexity whereas only coordinative complexity differentially affected the accuracy of relative phasing. The obtained performance measures were found to be significantly correlated with disease duration (unimanual) and with the score on the total motor scale, the Mini-Mental State Examination and the Stroop Interference Test (uni- and bimanual). After 12 months, maximal cycling frequency of unimanual elbow flexion–extension was significantly decreased in HD patients whereas the quality of the in-phase and anti-phase movement patterns remained stable. Electronic Publication     

Effects of age and fine motor expertise on the bilateral deficit in force initiation

Performance of a task carried out with two hands separately is better than the performance of the same task done with both hands at the same time. This so-called bilateral deficit may be reduced or counteracted by long-term practice. Little is known about age-related changes. We examined age- and expertise-related differences in the bilateral deficit in force initiation. Participants performed static and dynamic force modulation tasks either with the right and left hand separately or both hands simultaneously. In order to examine age-related differences, we compared novices of fine motor control (service employees) from three age groups, covering the working age (young n = 13, early middle-aged n = 10 and late middle-aged n = 12). To assess the influence of expertise, we considered precision mechanics as experts in fine motor control. To ensure the acquisition of expertise, only early middle-aged (n = 10) and late middle-aged (n = 14) experts were recruited. Regardless of the task, bimanual force initiation was slower than unimanual force initiation. This bilateral deficit was (1) more pronounced in the static than in the dynamic task, (2) higher in early and late middle-aged than in younger novices, and (3) lower in experts as compared to novices. Based on our results, we assume both interhemispheric inhibition and division of attention to contribute to the bilateral deficit and the expertise- and age-related differences, respectively. The results are promising for the possibility to overcome constraints of bilateral hand movements by long-term practice.     

Developmental changes in unimanual and bimanual aiming movements

The aim of this study was twofold: (a) analyze the development of reaction time (RT) and movement time (MT) for bimanual and unimanual movements and (b) investigate the interaction of age and sex on the changes in RT and MT. Participants (5-, 8-, and 11-year-olds) were asked to aim at target buttons under three conditions of movement: unimanual, bimanual symmetrical, and bimanual nonsymmetrical. As expected, RTs for bimanual symmetrical movements were shorter than RTs for unimanual and bimanual nonsymmetrical movements in the 5-year-olds. By the age of 8, bimanual nonsymmetrical movements still yielded longer RTs than unimanual and bimanual symmetrical movements, which no longer differed from each other. Regarding MT, in the 2 younger groups there was an advantage of unimanual over bimanual symmetrical movements. The latter were executed faster than nonsymmetrical movements at all ages. These results suggest that the evolution of RT and MT with age reflects development of interhemispheric transfer of information. It appears that the functional improvement of such transfer, which depends on the corpus callosum, progressively enables contralateral motor inhibition and the coordination of complex bilateral movements. The exchange of movement feedback information could mature more slowly than that of feed-forward information, explaining the extended time course of MT evolution.     

Unraveling interlimb interactions underlying bimanual coordination

Three sources of interlimb interactions have been postulated to underlie the stability characteristics of bimanual coordination but have never been evaluated in conjunction: integrated timing of feedforward control signals, phase entrainment by contralateral afference, and timing corrections based on the perceived error of relative phase. In this study, the relative contributions of these interactions were discerned through systematic comparisons of five tasks involving rhythmic flexion-extension movements about the wrist, performed bimanually (in-phase and antiphase coordination) or unimanually with or without comparable passive movements of the contralateral hand. The main findings were the following. 1) Contralateral passive movements during unimanual active movements induced phase entrainment to interlimb phasing of either 0 degrees (in-phase) or 180 degrees (antiphase). 2) Entrainment strength increased with the passive movements' amplitude, but was similar for in-phase and antiphase movements. 3) Coordination of unimanual active movements with passive movements of the contralateral hand (kinesthetic tracking) was characterized by similar bilateral EMG activity as observed in active bimanual coordination. 4) During kinesthetic tracking the timing of the movements of the active hand was modulated by afference-based error corrections, which were more pronounced during in-phase coordination. 5) Indications of in-phase coordination being more stable than antiphase coordination were most prominent during active bimanual coordination and marginal during kinesthetic tracking. Together the results indicated that phase entrainment by contralateral afference contributed equally to the stability of in-phase and antiphase coordination, and that differential stability of these patterns depended predominantly on integrated timing of feedforward signals, with only a minor role for afference-based error corrections.     

Functional synchronization in repetitive bimanual prehension movements

To examine the mechanisms of functional bimanual synchronization in goal-directed movements, we studied the movement kinematics of motorically unimpaired subjects while they performed repetitive prehension movements (either unimanually or bimanually) to small food items. Compared to unimanual conditions, bimanual movement execution yielded a significantly prolonged mouth contact phase. We hypothesized that this threefold prolongation led to a proper functional synchronization of the movement onsets of both hands at the beginning of each new movement cycle. That these temporal adjustments occurred in the movement phase with maximal haptic input points to the importance of sensory feedback for bimanual coordination. These results are discussed with respect to the important role of sensory feedback in the timing of coordinated bimanual movements. Furthermore, we propose that time-based coordinating schemas, which are implemented by the cerebellum and the posterior parietal cortex using sensory feedback, underlie functional inter-limb coordination.     

Structure of joint variability in bimanual pointing tasks

Changes in the structure of motor variability during practicing a bimanual pointing task were investigated using the framework of the uncontrolled manifold (UCM) hypothesis. The subjects performed fast and accurate planar movements with both arms, one moving the pointer and the other moving the target. The UCM hypothesis predicts that joint kinematic variability will be structured to selectively stabilize important task variables. This prediction was tested with respect to selective stabilization of the trajectory of the endpoint of each arm (unimanual control hypotheses) and with respect to selective stabilization of the timecourse of the vectorial distance between the target and the pointer tip (bimanual control hypothesis). Components of joint position variance not affecting and affecting a mean value of a selected variable were computed at each 10% of normalized movement time. The ratio of these two components ( R(V)) served as a quantitative index of selective stabilization. Both unimanual control hypotheses and the bimanual control hypothesis were supported both prior to and after practice. However, the R(V) values for the bimanual control hypothesis were significantly higher than for either of the unimanual control hypothesis, suggesting that the bimanual synergy was not simply a simultaneous execution of two unimanual synergies. After practice, an improvement in both movement speed and accuracy was accompanied by counterintuitive changes in the structure of kinematic variability. Components of joint position variance affecting and not affecting a mean value of a selected variable decreased, but there was a significantly larger drop in the latter when applied on each of the three selected task variables corresponding to the three control hypotheses. We conclude that the UCM hypothesis allows quantitative assessment of the degree of stabilization of selected performance variables and provides information on changes in the structure of a multijoint synergy that may not be reflected in its overall performance.     

The coordination patterns observed when two hands reach-to-grasp separate objects

What determines coordination patterns when both hands reach to grasp separate objects at the same time? It is known that synchronous timing is preferred as the most stable mode of bimanual coordination. Nonetheless, normal unimanual prehension behaviour predicts asynchrony when the two hands reach towards unequal targets, with synchrony restricted to targets equal in size and distance. Additionally, sufficiently separated targets require sequential looking. Does synchrony occur in all cases because it is preferred in bimanual coordination or does asynchrony occur because of unimanual task constraints and the need for sequential looking? We investigated coordinative timing when participants (n = 8) moved their right (preferred) hand to the same object at a fixed distance but the left hand to objects of different width (3, 5, and 7 cm) and grip surface size (1, 2, and 3 cm) placed at different distances (20, 30, and 40 cm) over 270 randomised trials. The hand movements consisted of two components: (1) an initial component (IC) during which the hand reached towards the target while forming an appropriate grip aperture, stopping at (but not touching) the object; (2) a completion component (CC) during which the finger and thumb closed on the target. The two limbs started the IC together but did not interact until the deceleration phase when evidence of synchronisation began to appear. Nonetheless, asynchronous timing was present at the end of the IC and preserved through the CC even with equidistant targets. Thus, there was synchrony but requirements for visual information ultimately yielded asynchronous coordinative timing.     

Single-unit activity related to bimanual arm movements in the primary and supplementary motor cortices

Single units were recorded from the primary motor (MI) and supplementary motor (SMA) areas of Rhesus monkeys performing one-arm (unimanual) and two-arm (bimanual) proximal reaching tasks. During execution of the bimanual movements, the task related activity of about one-half the neurons in each area (MI: 129/232, SMA: 107/206) differed from the activity during similar displacements of one arm while the other was stationary. The bulk of this "bimanual-related" activity could not be explained by any linear combination of activities during unimanual reaching or by differences in kinematics or recorded EMG activity. The bimanual-related activity was relatively insensitive to trial-to-trial variations in muscular activity or arm kinematics. For example, trials where bimanual arm movements differed the most from their unimanual controls did not correspond to the ones where the largest bimanual neural effects were observed. Cortical localization established by using a mixture of surface landmarks, electromyographic recordings, microstimulation, and sensory testing suggests that the recorded neurons were not limited to areas specifically involved with postural muscles. By rejecting this range of alternative explanations, we conclude that neural activity in MI as well as SMA can reflect specialized cortical processing associated with bimanual movements.     

Discrepancy in the involution of the different neural loops with age

The purpose of the study was to compare the effects of sensory manipulations on postural control for subjects of different ages. A young group of subjects (n = 17; 20.0 ± 1.3 years) and an old group of subjects (n = 17; 74.7 ± 6.3 years) were compared in 14 postural conditions [2 reference conditions and 12 sensory manipulation conditions: eyes closed, cervical collar, tendon vibration, electromyostimulation, galvanic vestibular stimulation (2 designs), foam surface] on a force platform. Spatio-temporal parameters of the center of foot pressure displacement were analyzed. When vestibular or proprioceptive afferences were manipulated, the old group was more disturbed than the young group. In addition, when myo-articular proprioceptive afferences were the only non-manipulated information source, the old group was also more disturbed than the young group. Hence, the inability to correctly interpret proprioceptive information and/or the impairment of myo-articular information would appear to be the major factor causing postural control deterioration. Moreover, concerning the vestibular system, it may be that aging alters the central integration of vestibular afferences. These results suggest that aging differently affects the functional ability of the different neural loops in postural control.     

Lack of age effects on human brain potentials preceding voluntary movements

We examined age effects on Movement related potentials (MRPs) in 13 young (mean age = 29.3 years) and 13 old (mean age = 67.2 years) normal adults in right, left and bimanual self-paced button press conditions. Both the groups generated a slowly rising readiness potential (RP) at about 1000 ms, a negative shift (NS') at about 450 ms and a motor potential (MP) at about 100 ms prior to movement. The RP was symmetrical, bilaterally distributed and maximal at the vertex in all conditions in both the groups. Both the groups produced contralaterally enhanced NS' and MP components in unimanual conditions. In contrast to prior reports, topographical distribution, onset latency and mean amplitude were comparable between young and old subjects for the RP, NS' and MP components of the MRP. The results indicate that motor programming as indexed by MRPs is unaffected by normal aging.     

Aging-related decline in somatosensory inhibition of the human cerebral cortex

Primary somatosensory (SI) cortical inhibition to repetitive stimuli tends to decline with increasing age. However, aging effects on the inhibition mechanism of secondary somatosensory cortex (SII) remain elusive. We aimed to study the aging-related changes of cortical inhibition in the human somatosensory system. Neuromagnetic responses to paired-pulse electrical stimulation to the median nerve were recorded in 21 young and 20 elderly male adults. Paired-pulse suppression (PPS) of SI and SII activities was estimated by the ratio of the response to Stimulus 2 to the response to Stimulus 1. Based on equivalent current dipole modeling, PPS ratios of the contralateral (SIIc) and ipsilateral (SIIi) secondary somatosensory cortices were higher in elderly than in young subjects (p < 0.001 in SIIc and p = 0.034 in SIIi). At an individual basis, a higher PPS ratio in SIIc than in SI was found in 16 (80 %) out of the 20 elderly participants; in contrast, the PPS ratios of SIIc and SI cortices were similar in young participants (p = 0.031). In conclusion, a larger PPS ratio in elderly suggests an aging-related decline in somatosensory cortical inhibition. Furthermore, compared to SI, the electrophysiological responses of SII cortex are especially vulnerable to aging in terms of cortical inhibition to repetitive stimulation.     

Tapping with intentional drift

When tapping a desired frequency, subjects tend to drift away from this target frequency. This compromises the estimate of the correlation between inter-tap intervals (ITIs) as predicted by the two-level model of Wing and Kristofferson which consists of an internal timer (‘clock’) and motor delays. Whereas previous studies on the timing of rhythmic tapping attempted to eliminate drift, we compared the production of three constant frequencies (1.5, 2.0, and 2.5 Hz) to the production of tapping sequences with a linearly decreasing inter-tap interval (ITI) (corresponding to an increase in tapping frequency from 1.5 to 2.5 Hz). For all conditions a synchronization–continuation paradigm was used. Tapping forces and electromyograms of the index-finger flexor and extensor were recorded and ITIs were derived yielding interval variability and model parameters, i.e., clock and motor variances. Electromyographic recordings served to study the influence of tapping frequency on the peripheral part of the tap event. The condition with an increasing frequency was more difficult to perform, as evidenced by an increase in deviation from the intended ITIs. In general, tapping frequency affected force level, inter-tap variability, model parameters, and muscle co-activation. Parameters for the condition with a decreasing ITI were comparable to those found in the constant frequency conditions. That is, although tapping with an intentional drift is different from constant tapping and more difficult to perform, the timing properties of both forms of tapping are remarkably similar and described well by the Wing and Kristofferson model.

Human superior parietal lobule is involved in somatic perception of bimanual interaction with an external object

The question of how the brain represents the spatial relationship between the own body and external objects is fundamental. Here we investigate the neural correlates of the somatic perception of bimanual interaction with an external object. A novel bodily illusion was used in conjunction with functional magnetic resonance imaging (fMRI). During fMRI scanning, seven blindfolded right-handed participants held a cylinder between the palms of the two hands while the tendon of the right wrist extensor muscle was vibrated. This elicited a kinesthetic illusion that the right hand was flexing and that the hand-held cylinder was shrinking from the right side. As controls, we vibrated the skin surface over the nearby bone beside the tendon or vibrated the tendon when the hands were not holding the object. Neither control condition elicited this illusion. The significance of the illusion was also confirmed in supplementary experiments outside the scanner on another 16 participants. The "bimanual shrinking-object illusion" activated anterior parts of the superior parietal lobule (SPL) bilaterally. This region has never been activated in previous studies on unimanual hand or hand-object illusion. The illusion also activated left-hemispheric brain structures including area 2 and inferior parietal lobule, an area related to illusory unimanual hand-object interaction between a vibrated hand and a touched object in our previous study. The anterior SPL seems to be involved in the somatic perception of bimanual interaction with an external object probably by computing the spatial relationship between the two hands and a hand-held object.     

Bimanual coordination and perceptual grouping in a patient with motor neglect

Motor neglect refers to the underutilisation of a limb contralateral to a brain lesion in the absence of primary motor and sensory deficits. The related problem of motor extinction refers to a contralesional motor deficit that worsens or only becomes apparent when bilateral actions are required. We present a single case (MM) of a patient with motor neglect who also demonstrates a form of motor extinction that is influenced by visual grouping between stimuli. The comparisons of unimanual and bimanual reach to grasp movements towards one or two objects in Experiment 1 showed that MM made relatively normal unimanual contralesional movements but impaired contralesional movements under bimanual action conditions. Experiment 2 demonstrated that motor extinction was improved by asking MM to make bimanual movements towards a single object. In Experiment 3, the effects of object coding on bimanual movement were replicated across conditions that varied the distance between end points for the movements. MM did not show overt visual extinction. We suggest that MM demonstrates a late-acting attentional bias that is expressed in terms of competitive motor activity. Normally, the contralesional limb "loses" the competition for action, but this can be modulated by visual grouping between targets.     

Bimanual coordination and perceptual grouping in a patient with motor neglect

Motor neglect refers to the underutilisation of a limb contralateral to a brain lesion in the absence of primary motor and sensory deficits. The related problem of motor extinction refers to a contralesional motor deficit that worsens or only becomes apparent when bilateral actions are required. We present a single case (MM) of a patient with motor neglect who also demonstrates a form of motor extinction that is influenced by visual grouping between stimuli. The comparisons of unimanual and bimanual reach to grasp movements towards one or two objects in Experiment 1 showed that MM made relatively normal unimanual contralesional movements but impaired contralesional movements under bimanual action conditions. Experiment 2 demonstrated that motor extinction was improved by asking MM to make bimanual movements towards a single object. In Experiment 3, the effects of object coding on bimanual movement were replicated across conditions that varied the distance between end points for the movements. MM did not show overt visual extinction. We suggest that MM demonstrates a late-acting attentional bias that is expressed in terms of competitive motor activity. Normally, the contralesional limb “loses” the competition for action, but this can be modulated by visual grouping between targets.