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.     

Suboptimal online control of aiming movements in virtual contexts

We determined whether uncertainty about the location of one’s hand in virtual environments limits the efficacy of online control processes. In the Non-aligned and Aligned conditions, the participant’s hand was represented by a cursor on a vertical or horizontal display, respectively. In the Natural condition, participants saw their hand. During an acquisition phase, visual feedback was either permitted or not during movement execution. To test the hypothesis (Norris et al. 2001) that reliance on visual feedback increases as the task becomes less natural (Natural < Aligned < Non-aligned), following acquisition, participants performed a transfer phase without visual feedback. During acquisition in both visual feedback conditions, movement endpoint variability increased as the task became less natural. This suggests that the orientation of the display and the representation of one’s hand by a cursor introduced uncertainty about its location, which limits the efficacy of online control processes. In contradiction with the hypothesis of Norris et al. (2001), withdrawing visual feedback in transfer had a larger deleterious effect on movement accuracy as the task became less natural. This suggests that the CNS increases the weight attributed to the input that can be processed without first having to be transformed.     

Visual–spatial and anatomical constraints interact in a bimanual coordination task with transformed visual feedback

There is a debate in the literature about the influence of spatial and anatomical constraints on bimanual coordination dynamics. In the present experiment, participants swung hand-held pendulums about the wrist while attending to visual feedback about relative phase (superimposed phase plots of each pendulum) that was displayed on a screen. Participants were instructed to maintain in-phase or anti-phase coordination in the visual display. Visual–spatial and anatomical constraints were dissociated by introducing a phase shift in the visual display so that visual feedback differed from the movements being performed by the participants in 15° increments from −180° to +180°. Analysis of mean relative phase and its variability suggested that visual–spatial and anatomical constraints interact in bimanual coordination dynamics.     

Exploring coordination dynamics of the postural system with real-time visual feedback

Differential performance over a wide range of possible postural coordination modes was investigated using 16 ankle-hip relative phase patterns from 0 degrees to 337.5 degrees. Participants were instructed to produce each coordination mode with and without real time visual feedback. Feedback consisted of a Lissajous figure indicating the discrepancy between actual and requested ankle-hip relative phase. The results showed: (1) the presence of a unique attractor around the anti-phase pattern (relative phase approximately 180 degrees); (2) performance was similar with and without visual feedback; (3) the absence of an attractor for the in-phase pattern (relative phase approximately 20 degrees). The third result is not consistent with previous research in which both in-phase and anti-phase patterns emerged when they were not imposed [B.G. Bardy, L. Martin, T.A. Stoffregen, R.J. Bootsma, Postural coordination modes considered as emergent phenomena, J. Exp. Psychol. Hum. Percept. Perform. 25 (1999) 1284-1301; B.G. Bardy, O. Oullier, R.J. Bootsma, T.A. Stoffregen, Dynamics of human postural transitions, J. Exp. Psychol. Hum. Percept. Perform. 28 (1999) 499-514]. This finding indicates the strong dependency to task variation and instructions of postural pattern formation.     

High-frequency transcranial magnetic stimulation of the supplementary motor area reduces bimanual coupling during anti-phase but not in-phase movements

Previous electrophysiological and neuroimaging studies have provided evidence that the supplementary motor area (SMA) has an important role in the control of bimanual coordination. The present experiment investigated the effects of high-frequency repetitive transcranial magnetic stimulation (rTMS) over the SMA region on kinematic variables during cyclical bimanual coordination, with a particular focus on the quality of coordination. Subjects performed metronome-paced trials of in-phase and anti-phase bimanual index-finger movements at near-maximal cycling frequency. During movement execution, rTMS (20 Hz, 0.5 s, 120% hand motor threshold) was applied over one of three positions in the sagittal midline 2.0, 4.0 and 6.0 cm anterior to the primary motor leg area. Sham rTMS was included as a control condition. After rTMS, the mean relative phase error between hands increased, but only in the anti-phase trials. The maximum increase in phase error occurred immediately after rather than during the rTMS train. The effect was largest after stimulation 4 or 6 cm anterior to the leg area of the primary motor cortex. We did not observe any changes in the variability of relative phase or in cycle duration or movement amplitude. Findings are discussed in light of recent functional models on the role of the SMA in bimanual movement control.     

Interlimb coordination in patients with Parkinson’s disease: motor learning deficits and the importance of augmented information feedback

 The basal ganglia have traditionally been associated with motor control functions and this view has prevailed since the late nineteenth century. Recent experimental studies suggest that this neuroanatomical system is also critically involved in motor learning. In the present study, motor learning/transfer capabilities were compared between patients with Parkinson’s disease and a group of normal elderly people. Subjects practiced a bimanual coordination task that required continuous flexion-extension movements in the transverse plane with a 90° phase offset between the forearms. During acquisition, augmented visual feedback of the relative motions was provided in real time. The findings revealed improvements in the bimanual coordination pattern across practice in both groups when the augmented concurrent feedback was present. However, when transferred to performance conditions in which the augmented information was withheld, performance deteriorated (relative to the augmented condition) and this effect was more prevalent in the Parkinson patients. More specifically, no improvement in interlimb coordination was observed under nonaugmented feedback conditions across practice. Instead, a drift toward the preferred in-phase and anti-phase coordination patterns was evident. The present findings suggest that Parkinson patients can improve their performance on a new motor task, but they remain strongly dependent on augmented visual information to guide these newly acquired movements. The apparent adoption of a closed-loop control mode is accompanied with decreases in movement speed in order to use the feedback to ensure accuracy. When the augmented feedback is withheld and the movement pattern is to be controlled by means of intrinsic information feedback sources, performance is severely hampered. The findings are hypothesized to indicate that learning/transfer is affected in Parkinson patients who apparently prefer some constancy in the environmental contingencies under which practice takes place. The present findings are consistent with the notion that the basal ganglia form a critical neuroanatomical substrate for motor learning. Received: 7 December 1995 / Accepted: 12 August 1996     

Influence of an exhausting muscle exercise on bimanual coordination stability and attentional demands

The present study investigated the influence of a bilateral exhaustive exercise on the stability of bimanual anti-phase coordination pattern and attentional demands. Eight subjects performed the anti-phase coordination pattern in two sessions: an Exhausting Session and a Control Session. During the Exhausting Session, subjects performed the bimanual coordination after exhaustion of forearms muscles (i.e. endurance time test). For the Control Session, no endurance time test was previously designed before the performance of anti-phase coordination. Within these experimental sessions, two levels of load (loaded and unload) and two frequencies (1.75 and 2.25 Hz) were also manipulated during the bimanual task. Attentional demands associated with performing the anti-phase coordination pattern was measured via a probe reaction time task (RT). The results showed that relative phase variability was higher for the fastest frequency after the exhaustive exercise. Moreover, as a result of the previous muscle exercise, the observed phase coupling was less accurate. No significant effect was found concerning the attentional demands as assessed through RT. The present findings suggest that the muscle exhaustion affects bimanual performance at a more peripheral level.     

Location but not amount of stimulus occlusion influences the stability of visuo-motor coordination

The current study examined whether the amount and location of available movement information influenced the stability of visuo-motor coordination. Participants coordinated a hand-held pendulum with an oscillating visual stimulus in an inphase and antiphase manner. The effects of occluding different amounts of phase at different phase locations were examined. Occluding the 0°/180° phase locations (end-points) significantly increased the variability of the visuo-motor coordination. The amount of occlusion had little or no affect on the stability of the coordination. We concluded that the end-points of a visual rhythm are privileged and provide access to movement information that ensures stable coordination. The results are discussed with respect to the proposal of Bingham and colleagues (e.g., Bingham GP. Ecol Psychol 16:45–53, 2004a; Wilson AD, Collins DR, Bingham GP. Exp Brain Res 165:351–361, 2005a) that the relevant information for rhythmic visual coordination is relative direction information.     

Disruption of bilateral temporal coordination during arm swinging in patients with hemiparesis

Persistent motor deficits in the paretic arm present a major barrier to the recovery of the ability to perform bimanual tasks even in individuals who have recovered well after a stroke. Impaired performance may be related to deficits in bimanual temporal coordination due to stroke-related damage of specific brain motor structures as well as changed biomechanics of the paretic arm. To determine the extent of the deficit in bilateral temporal coordination after the stroke, we investigated how bilateral reciprocal coordination was regained after external perturbations of the arm in individuals with hemiparesis due to stroke. We used a bilateral task that would be minimally affected by the unilateral arm motor deficit. Nine non-disabled control subjects and 12 individuals with chronic hemiparesis performed reciprocal (anti-phase) arm swinging in the standing position for 15 s per trial. In each trial, movement of one arm was unexpectedly and transiently (~150–350 ms) arrested at the level of the wrist once in the forward and once in the backward phase of swinging. Perturbation was applied to the left and right arms in control subjects and to the paretic and non-paretic arms of individuals with hemiparesis. Kinematic data from endpoint markers on both hands and electromyographic activity of anterior and posterior deltoid muscles from both arms were recorded. The oscillatory period, the phase differences between arms and the mean EMG activity before, during and after perturbation were analyzed. In both groups the perturbation altered the period of the perturbed cycle in both the arrested and non-arrested arms and resulted in a change from anti-phase to in-phase coordination, following which anti-phase coordination was regained. Recovery of anti-phase swinging took significantly longer in patients with hemiparesis compared to control subjects. Stable pre-perturbed (anti-phase) reciprocal coordination was regained within one cycle following perturbation for the control subjects and within two cycles following perturbation for the patients with hemiparesis. Analysis of EMG activation levels showed that, compared to control subjects, there was significantly less activation of the shoulder muscles in response to perturbation in the patient group and the pattern of muscle activation in the paretic arm was opposite to that in the non-paretic and control arms. The finding that patients had a reduced capacity for maintaining and restoring the required reciprocal coordination when perturbation occurred suggests that stroke-related brain damage in our patients led to instability of bilateral temporal coordination for this rhythmical task.     

The stability of rhythmic movement coordination depends on relative speed: the Bingham model supported

Following many studies showing that the coupling in bimanual coordination can be perceptual, Bingham (Ecol Psychol in 16:45–53, 2001; 2004a, b) proposed a dynamical model of such movements. The model contains three key hypotheses: (1) Being able to produce stable coordinative movements is a function of the ability to perceive relative phase, (2) the information to perceive relative phase is relative direction of motion, and (3) the ability to resolve this information is conditioned by relative speed. The first two hypotheses have been well supported (Wilson and Bingham in Percept Psychophys 70:465–476, 2008; Wilson et al. in J Exp Psychol Hum 36:1508–1514, 2010a), but the third was not supported when tested by de Rugy et al. (Exp Brain Res 184:269–273, 2008) using a visual coordination task that required simultaneous control of both the amplitude and relative phase of movement. The purposes of the current study were to replicate this task with additional measures and to modify the original model to apply it to the new task. To do this, we conducted two experiments. First, we tested the ability to produce 180° visual coordination at different frequencies to determine frequencies suitable for testing in the de Rugy et al. task. Second, we tested the de Rugy et al. task but included additional measures that yielded results different from those reported by de Rugy et al. These results were used to elaborate the original model. First, one of the phase-driven oscillators was replaced with a harmonic oscillator, so the resulting coupling was unidirectional. This change resulted in the model producing less stable 180° coordination behavior beyond 1.5 Hz consistent with the results obtained in Experiment 1. Next, amplitude control and phase correction elements were added to the model. With these changes, the model reproduced behaviors observed in Experiment 2. The central finding was that the stability of rhythmic movement coordination does depend on relative speed and, thus, all three of the hypotheses contained in the original Bingham model are supported.     

Bimanual Fitts’ tasks: Kelso,Southard, and Goodman, 1979 revisited

The experiment was designed to replicate and extend to an integrated feedback condition the pattern of movement time results found by Kelso et al. (J Exp Psychol Hum Percept Perform 5:229–238, 1979a, Science 204:1029–1031, 1979b) where the simultaneous movement of one hand to a low ID target and the other to a higher ID target indicated “a tight coordinate coupling between the hands” (p. 229). In the present experiment, a control group was provided feedback that depicted the independent movement of the two limbs under low and higher indexes of difficulty (ID). A Lissajous group was provided integrated feedback in the form of a Lissajous plot. The results indicated a pattern of results for the control and Lissajous groups similar to that found by Kelso et al. for one and two-limb movements to the same difficulty targets. The control group also replicated the finding for two-limb movements to mixed ID tasks. However, the Lissajous group simultaneously produced disparate movement in the mixed target conditions. The results are consistent with recent findings indicating that when provided salient integrated feedback participants can effectively produce disparate movements of the two limbs.     

The role of proprioception in the control of prehension movements: a kinematic study in a peripherally deafferented patient and in normal subjects

In this study we investigated the role of proprioception in the control of prehension movements, with particular reference to the grasp component. Grasp and transport kinematics were studied in a peripherally deafferented patient and in five healthy subjects. Two experiments were carried out: the prehension experiment and the grasp perturbation experiment. In the prehension experiment both the patient and the control subjects were required to reach and grasp three objects of different size, located at three different distances, both with and without visual feedback. In the grasp perturbation experiment a mechanical perturbation was applied to the fingers during prehension movements, again executed with and without visual feedback. In the prehension experiment temporal parameters of the patient's movements were generally slowed, with greater variability on some measures. However, over the first phase of the movement the pattern of the patient's hand opening and transport acceleration, scaled to object size and distance, was the same as that of controls, both with and without visual feedback. On the contrary, during the final phase of the movement (the finger closure phase and deceleration) the patient's performance differed significantly from the controls. These phases were abnormally lengthened and frequent movement adjustments were observed. In the grasp perturbation experiment the patient was not able to compensate for the perturbations applied to the fingers, even with visual feedback. The data allowed us to investigate also the respective contribution of proprioception and of vision of the hand in the control of prehension. We compared prehension kinematics in two conditions: (a) with visual but no proprioceptive feedback (in the patient) and (b) with proprioceptive but no visual feedback (in the controls). In both experiments proprioceptive control was more efficient than visual control. The results of this study are interpreted in favour of the strict dependence of prehension control on proprioception. The first phase of the movement, however, can be appropriately planned and executed without the necessity of either proprioceptive or visual information about the hand.     

The Brentano illusion influences goal-directed movements of the left and right hand to the same extent

Recently, Gonzalez et al. (J Neurophys 95:3496–3501, 2006) reported that movements with the left hand are more susceptible to visual size illusions than are those with the right hand. We hypothesized that this might be because proprioceptive information about the position of the left hand is less precise. If so, the difference between the hands should become clearer when vision of the hand is removed so that subjects can only rely on proprioception to locate their hand. We tested whether this was so by letting right-handed subjects make open-loop pointing movements within an illusory context with and without vision of their hand. On average, the illusion influenced the left and the right hand to the same extent, irrespective of the visibility of the hand. There were some systematic differences between the hands within certain regions of space, but these were not consistent across subjects. We conclude that there is no fundamental difference between the hands in susceptibility to the Brentano illusion.     

Stability of rhythmic visuo-motor tracking does not depend on relative velocity

It is well established that the in-phase pattern of bimanual coordination (i.e. a relative phase of 0°) is more stable than the antiphase pattern (i.e., a relative phase of 180°), and that a spontaneous transition from antiphase to in-phase typically occurs as the movement frequency is gradually increased. On the basis of results from relative phase perception experiments, Bingham (Proceedings of the 23rd annual conference of the cognitive science society. Laurence Erlbaum Associates, Mahwah, pp 75–79, 2001; Ecol Psychol 16:45–53, 2004; Advances in psychology 135: time-to-contact. Elsevier, Amsterdam, pp 421–442, 2004) proposed a dynamical model that consists of two phase driven oscillators coupled via the perceived relative phase, the resolution of which is determined by relative velocity. In the present study, we specifically test behavioral predictions from this last assumption during a unimanual visuo-motor tracking task. Different conditions of amplitudes and frequencies were designed to manipulate selectively relative phase and relative velocity. While the known effect of phase and frequency were observed, relative phase variability was not affected by the different conditions of relative velocity. As such, Bingham’s model assumption that instability in relative phase coordination is brought about by relative velocity that affects the resolution of the perceived relative phase has been invalidated for the case of rhythmic unimanual visuo-motor tracking. Although this does not rule out the view that relative phase production is constrained by relative phase perception, the mechanism that would be responsible for this phenomenon still has to be established.     

Using scanning trials to assess intrinsic coordination dynamics

Bimanual 1:1 coordination patterns other than in-phase (0°) and anti-phase (180°) have proven difficult to perform even with extended practice. The difficulty has been attributed to phase attraction that draws the coordination between the limbs towards the bimanual patterns of in-phase and anti-phase and variability associated with the activation of non-homologous muscles via crossed and uncrossed cortical pathways. We found participants could very effectively produce a large range of supposedly unstable coordination patterns (between 0° and 180° in 30° increments) after only 3 min of practice when integrated feedback (Lissajous plots) was provided and other perceptual and attentional distractions were minimized. These findings clearly indicate that the perception-action system is fully capable of producing a wide range of bimanual coordination patterns and that the reason for the failure to produce these patterns in previous experiments reside in the perceptual information and attentional requirements typically found in experimental testing environments.     

Changes in tremor as a function of type of augmented visual information

The dynamics of postural finger tremor is typically investigated under conditions of natural vision of the finger. Here we investigated the effect of different types of augmented visual information feedback on finger tremor and on inter-limb tremor coordination. Four visual information conditions of postural finger tremor from either the dominant hand only or from both hands were investigated. The visual conditions were: (1) no vision, (2) natural vision, (3) augmented vision with instantaneous acceleration on a computer display, and (4) augmented vision with instantaneous and past acceleration on a computer display. Acceleration was measured with a 3D accelerometer on the distal phalanx of the index finger(s). The amount of tremor variability did not change as a function of visual information conditions. However, removing visual feedback increased tremor predictability and reduced small, random deviations of tremor acceleration output in the one finger condition. In the two-finger condition, augmented visual information increased the irregularity of the combined tremor variability. The no vision condition showed a stronger coupling between fingers than natural vision or augmented vision with past information. The findings revealed that augmented visual information increased tremor irregularity and facilitated coupling in two-hand tremor dynamics.     

Factors affecting higher-order movement planning: a kinematic analysis of human prehension

Summary Past studies of the kinematics of human prehension have shown that varying object size affects the maximum opening of the hand, while varying object distance affects the kinematic profile of the reaching limb. These data contributed to the formulation of a theory that the reaching and grasping components of human prehension reflect the output of two independent, though temporally coupled, motor programs (Jeannerod 1984). In the first experiment of the present study, subjects were required to reach out and grasp objects, with or without on-line, visual feedback. Object size and distance were covaried in a within-subjects design, and it was found that both grip formation and reach kinematics were affected by the manipulation of either variable. These data suggest that the control mechanisms underlying transport of the limb and grip formation are affected by similar task constraints. It was also observed that when visual feedback was unavailable after movement onset subjects showed an exaggerated opening of their hands, although grip size continued to be scaled for object size. The question remained as to whether the larger opening of the hand during no-feedback trials reflected the lack of opportunity to fine-tune the opening of the hand on-line, or the adoption of a strategy designed to increase tolerance for initial programming errors. To address this question, a second experiment was carried out in which we manipulated the predictability of visual feedback by presenting feedback and no-feedback trials in a random order. In contrast to the situation in which feedback and no-feedback trials were presented in separate blocks of trials (Exp. 1), in the randomly ordered series of trials presented in Exp. 2, subjects always behaved as if they were reaching without vision, even on trials where visual feedback was continuously available. These findings suggest that subjects adopt different strategies on the basis of the predictability of visual feedback, although there is nothing to suggest that this takes place at a conscious, or voluntary, level. The results of both experiments are consistent with the notion of a hierarchically-organized motor control center, responsible for optimizing performance under a variety of conditions through the coordination of different effector systems and the anticipation of operating constraints.     

The relative effects of external spatial and motoric factors on the bimanual coordination of discrete movements

The ability to coordinate the two hands effectively is a fundamental requirement for many everyday tasks. To investigate how bimanual coordination is achieved we asked subjects to perform discrete bimanual key-press responses under conditions in which the motoric (i.e., muscles employed) and external spatial (i.e., direction of movement in external space) relationships between the actions of the left and right index fingers were systematically varied. Subjects made simultaneous right and left index finger key-presses in response to an auditory tone. The right finger always made downward flexion movements whilst the left finger either flexed in a downward/upward direction, or extended in a downward/upward direction. Unimanual control trials of each movement type for both hands were also performed. Reaction times for each hand (RTs) and the inter-response interval (IRI) were recorded . Right hand RTs were significantly affected only when the left finger performed motorically different actions, but were unaffected by the external spatial direction in which the left hands actions were made. The IRI results followed a similar pattern with the worst coordination (highest IRI) occurring when the left finger performed different motor actions to the right finger regardless of the direction of the left hand movement. In contrast to other recent results from experiments examining oscillatory tasks (e.g., Mechsner et al. 2001), our results suggest that in discrete tasks there is a dominance of the motor relationship between the hands over the external spatial relationship.     

Fooling the brain into thinking it sees both hands moving enhances bimanual spatial coupling

This study examined the hypothesis that the mirror reflection of one hands movement directly influences motor output of the other (hidden) hand, during performance of bimanual drawing. A mirror was placed between the two hands during bimanual circle drawing, with one hand and its reflection visible and the other hand hidden. Bimanual spatial coupling was enhanced by the mirror reflection, as shown by measures of circle size. Effects of the mirror reflection differed significantly from effects of vision to one hand alone, but did not differ from a control task performed in full vision. There was no evidence of a consistent phase lead of the visible hand, which indicates that the observed effects on spatial coupling were immediate and not based on time-consuming feedback processes. We argue that visual mirror symmetry fools the brain into believing it sees both hands moving rather than one. Consequently, the spatial properties of movement of the two hands become more similar through a process that is virtually automatic.     

Ipsilesional disruptions to reciprocal finger tapping.

Impairments in repetitive finger tapping have not been found in the ipsilesional hand, possibly because the performance measure (tapping rate) which has been used is not sufficiently sensitive. In this study, tapping performance of patients with lateralized brain damage was examined using more detailed measures reflecting intertap variability and the relative timing of each tap cycle. In concert with previous findings, neither the left- nor the right-hemisphere-damaged patients exhibited an impairment in tapping rate. An impairment in tapping variability was observed, however, but only for the left hemisphere group. It is argued that intertap variability may be particularly sensitive to left hemisphere damage as this measure reflects the demands for rather precise and consistent phasing or sequencing of muscle activation. Since left hemisphere damage often leads to deficits in making transitions between movements in a sequence, the consistent sequencing of agonist-antagonist muscle activations in tapping may be compromised. Future research directions to examine this hypothesis are discussed.