Mirror,mirror on the wall: viewing a mirror reflection of unilateral hand movements facilitates ipsilateral M1 excitability

Primary motor cortex (M1) excitability is modulated by both ipsilateral limb movement and passive observation of movement of the contralateral limb. An interaction of these effects within M1 may account for recent research suggesting improved functional recovery of the impaired arm following stroke by viewing a mirror reflection of movements of the unimpaired arm superimposed over the (unseen) impaired arm. This hypothesis was tested in the present study using single-pulse transcranial magnetic stimulation (TMS) in eight neurologically healthy subjects. Excitability of M1 ipsilateral to a phasic, unilateral hand movement was measured while subjects performed paced (1 Hz), unilateral index finger-thumb opposition movements. Motor evoked potentials (MEPs) were obtained from the inactive first dorsal interosseous (FDI) in each of four viewing conditions: Active (viewing the active hand), Central (viewing a mark positioned between hands), Inactive (viewing the inactive hand) and Mirror (viewing a mirror-reflection of the active hand in a mirror oriented in the mid-sagittal plane) and with both hands at rest (Rest). MEPs were significantly enhanced during ipsilateral hand movement compared with the Rest condition (P<0.05). Largest MEPs were obtained in the Mirror condition, and this was significant compared with both the Inactive and Central viewing conditions (P<0.05). There was no difference between the dominant and non-dominant hand. Excitability of M1 ipsilateral to a unilateral hand movement is facilitated by viewing a mirror reflection of the moving hand. This finding provides neurophysiological evidence supporting the application of mirror therapy in stroke rehabilitation.     

Visual guidance during an interception task in children with Spastic Hemiparetic Cerebral Palsy

The aims of the study are to determine the presence of adjustments in walking behaviour of children with Spastic Hemiparetic Cerebral Palsy (SHCP) during the interception of a moving ball and, whether the angle between the ball and the participant is kept constant. This would support the use of the so-called bearing angle (BA) strategy in interception of the object. Children with left hemisphere damage intercepted a ball from a conveyor belt at three different velocities, from a frontal or lateral orientation and with their impaired or less-impaired hand. The participants walked from a distance of 4 m perpendicularly to the belt. Children seemed to have less successful trials when grasping with the impaired hand. The results showed that the walking velocity was adjusted to the ball velocity. When they grasped with the impaired hand, children initially moved faster to the interception point, while closer to the belt significant slower. The BA showed less variation over the trajectory when the children grasped with their less-impaired hand or when the ball velocity increased. It was concluded that children with SHCP were able to take their impairment into account as indicated by adjustments in walking behaviour. However, these adjustments in walking velocity were not sufficient to compensate totally for the limited reaching ability in the impaired hand. As a result of these adjustments, the amount of variation from the constant BA seemed to deviate more from typically developing children when grasping with impaired hand than when grasping with less-impaired hand.     

The effect of visuomotor displacements on arm movement paths

The gently curved paths evident in point-to-point arm movements have been attributed to both an imperfect execution of a planned straight-hand path or as an emergent property of a control strategy in which an intrinsic cost, dependent on arm dynamics, is minimised. We used a virtual visual feedback system to test whether path curvature was mainly determined by the visually perceived or actual location of the moving limb. Hand paths were measured for movements between three pairs of targets under both veridical and uniformly translated visual feedback. This allowed us to decouple the actual and perceived hand location during movement. Under different conditions of visual feedback the curvature of the hand paths did not correlate with either the visually perceived location of the limb or the actual location but rather with the relative displacement between the actual and visually perceived limb locations. The results are consistent with the hypothesis that in planning a movement the internal estimate of intrinsic coordinates, such as joint angles, is at least partially derived from visual information. Received: 31 August 1998 / Accepted: 8 March 1999     

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.     

Postural adjustments for online corrections of arm movements in standing humans

The aim of this study was to investigate how humans correct ongoing arm movements while standing. Specifically, we sought to understand whether the postural adjustments in the legs required for online corrections of arm movements are predictive or rely on feedback from the moving limb. To answer this question we measured online corrections in arm and leg muscles during pointing movements while standing. Nine healthy right-handed subjects reached with their dominant arm to a visual target in front of them and aligned with their midline. In some trials, the position of the target would switch from the central target to one of the other targets located 15°, 30°, or 45° to the right of the central (midline) target. For each target correction, we measured the time at which arm kinematics, ground reaction forces, and arm and leg muscle electromyogram significantly changed in response to the target displacement. Results show that postural adjustments in the left leg preceded kinematic corrections in the limb. The corrective postural muscle activity in the left leg consistently preceded the corrective reaching muscle activity in the right arm. Our results demonstrate that corrections of arm movements in response to target displacement during stance are preceded by postural adjustments in the leg contralateral to the direction of target shift. Furthermore, postural adjustments preceded both the hand trajectory correction and the arm-muscle activity responsible for it, which suggests that the central nervous system does not depend on feedback from the moving arm to modify body posture during voluntary movement. Instead, postural adjustments lead the online correction in the arm the same way they lead the initiation of voluntary arm movements. This suggests that forward models for voluntary movements executed during stance incorporate commands for posture that are produced on the basis of the required task demands.     

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.     

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.     

Concurrent adaptations of left and right arms to opposite visual distortions

Previous research has shown that subjects can adapt with either arm to an opposite visual distortion, and the two adaptive states can then be used in sequence to control the respective arm. To extend this finding, we exposed the left and right arms of our subjects to opposite-directed rotations of the visual field alternately for 20 s each, and determined the time-course of adaptation, as well as aftereffects without visual feedback under uni- and bimanual conditions. Our data confirm that two adaptive states can co-exist in the sensorimotor system, one for each arm. We further found that the time-course of adaptive improvement was similar for both arms, that the improvement was present as early as the first movement after a change of arm and discordance, and that the magnitude of adaptation was similar to control data yielded by a single arm and discordance. Taken together, these findings suggest that the two adaptive states were formed concurrently, and without mutual interference. We also observed significant aftereffects. They were smaller but still appreciable under bimanual conditions; the two arms moved at the same time in different directions even though they were aimed at a common visual target. This outcome indicates that the two adaptive states were not merely of a strategic nature, but rather changed the rules by which sensory information was transformed into motor outputs; it also suggests that the two states not only co-exist, but can also be engaged concurrently in movement control. The reduced aftereffects observed under bimanual conditions can be attributed to the well-known phenomenon of bimanual coupling, which is unrelated to adaptation.     

Bimanual adaptation: internal representations of bimanual rhythmic movements

From tying your shoes and clipping your tie to the claps at the end of a fine seminar, bimanual coordination plays a major role in our daily activities. An important phenomenon in bimanual coordination is the predisposition toward mirror symmetry in the performance of bimanual rhythmic movements. Although learning and adaptation in bimanual coordination are phenomena that have been observed, they have not been studied in the context of adaptive control and internal representations—approaches that were successfully employed in the arena of reaching movements and adaptation to force perturbations. In this paper we examine the dynamics of the learning mechanisms involved when subjects are trained to perform a bimanual non-harmonic polyrhythm in a bimanual index finger tapping task. Subjects are trained in this task implicitly, using altered visual feedback, while their performance is continuously monitored throughout the experiment. Our experimental results indicate the existence of significant (p<<0.01) learning curves (i.e., error plots with significantly negative slopes) during training and aftereffects with a washout period after the visual feedback ceases to be altered. These results confirm the formation of internal representations in bimanual motor control. We present a simple, physiologically plausible, neural model that combines feedback and adaptation in the control process and which is able to reproduce key phenomena of bimanual coordination and adaptation.     

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.     

Upper limb asymmetries in the matching of proprioceptive versus visual targets

The purpose of the current study was to determine the extent to which "sensory dominance" exists in right-handers with respect to the utilization of proprioceptive versus visual feedback. Thirteen right-handed adults performed two target-matching tasks using instrumented manipulanda. In the proprioceptive matching task, the left or right elbow of blindfolded subjects was passively extended by a torque motor system to a target position and held for 3 s before being returned to the start position. The target angle was then matched with either the ipsilateral or contralateral arm. In the second task, visual matching, circular targets were briefly projected to either side of a visual fixation point located in front of the subject. Subjects then matched the target positions with a laser pointer by moving either the ipsilateral or contralateral arm. Overall, marked arm differences in accuracy were seen based on the type of sensory feedback used for target presentation. For the proprioceptive matching task errors were smaller for the nonpreferred left arm, whereas during the visual matching task smaller errors were found for the preferred right arm. These results suggest a left arm/right hemisphere advantage for proprioceptive feedback processing and a right arm/left hemisphere advantage for visual information processing. Such asymmetries may reflect fundamental differences between the two arm/hemisphere systems during the performance of bimanual tasks where the preferred arm requires visual guidance to manipulate an object, whereas the nonpreferred stabilizes that object on the basis of proprioceptive feedback.     

Saccade adaptation in response to altered arm dynamics

The delays in sensorimotor pathways pose a formidable challenge to the implementation of stable error feedback control, and yet the intact brain has little trouble maintaining limb stability. How is this achieved? One idea is that feedback control depends not only on delayed proprioceptive feedback but also on internal models of limb dynamics. In theory, an internal model allows the brain to predict limb position. Earlier we had found that during reaching, the brain estimates hand position in real-time in a coordinate system that can be used for generating saccades. Here we tested the idea that the estimate of hand position, as expressed through saccades, depends on an internal model that adapts to dynamics of the arm. We focused on the behavior of the eyes as perturbations were applied to the unseen hand. We found that when the hand was perturbed from stable posture with a 100-ms force pulse of random direction and magnitude, a saccade was generated on average at 182 ms postpulse onset to a position that was an unbiased estimate of real-time hand position. To test whether planning of saccades depended on an internal model of arm dynamics, arm dynamics were altered either predictably or unpredictably during the postpulse period. When arm dynamics were predictable, saccade amplitudes changed to reflect the change in the arm's behavior. We suggest that proprioceptive feedback from the arm is integrated into an adaptable internal model that computes an estimate of current hand position in eye-centered coordinates.     

Natriuretic peptides, but not nitric oxide donors, elevate levels of cytosolic guanosine 3',5'-cyclic monophosphate in ependymal cells ex vivo

We examined how children with Spastic Hemiparetic Cerebral Palsy (SHCP) perform interceptive actions they experience in daily life. Children were required to walk towards and intercept a stationary ball or a moving ball, with either their impaired or non-impaired arm. In the stationary ball condition the child was free to determine the speed of their response (internal timing), whereas in the moving ball condition there was a restricted time available (external timing). It was found that the reach movements of the non-impaired arm were different to the impaired arm, and were characterized by some of the typical movement limitations imposed by SHCP. However, there was no evidence of increased contribution from trunk motion or a lengthening of reach movement time or deceleration time. Instead, there was a coordinated change with the walking kinematics, whereby the children spent proportionately more time slowing down as they approached the point of interception when reaching with the impaired arm. There were also several differences in the response when intercepting a moving ball compared to a stationary ball. When the timing constraints were imposed externally (moving ball) rather than internally (stationary ball), children reached with a reduced movement time and deceleration time, and an increased peak wrist velocity and elbow excursion. These adaptations to behaviour were necessary to deal with the restricted time available to make the interception in the moving ball condition compared to when the ball was stationary, and reveal how children with SHCP coordinate walking and reaching when performing natural interceptive actions.     

Multi-frequency arm cycling reveals bilateral locomotor coupling to increase movement symmetry

Upright stance has allowed for substantial flexibility in how the upper limbs interact with each other: the arms can be coordinated in alternating, synchronous, or asymmetric patterns. While synchronization is thought to be the default mode of coordination during bimanual movement, there is little evidence for any bilateral coupling during locomotor-like arm cycling movements. Multi-frequency tasks have been used to reveal bilateral coupling during bimanual movements, thus here we used a multi-frequency task to determine whether the arms are coupled during arm cycling. It was hypothesized that bilateral coupling would be revealed as changes in background EMG and cutaneous reflexes when temporal coordination was altered. Twelve subjects performed arm cycling at 1 and 2 Hz with one arm while the contralateral arm was either at rest, cycling at the same frequency, or cycling at a different frequency (i.e., multi-frequency cycling with one arm at 1 Hz and the other at 2 Hz). To evoke reflexes, the superficial radial nerve was stimulated at the wrist. EMG was collected continuously from muscles of both arms. Results showed that background EMG in the lower frequency arm was amplified while reflex amplitudes were unaltered during multi-frequency cycling. We propose that neural coupling between the arms aids in equalizing muscle activity during asymmetric tasks to permit stable movement. Conversely, such interactions between the arms would likely be unnecessary in determining a reflexive response to a perturbation of one arm. Therefore, bilateral coupling was expressed when it was relevant to symmetry.     

Disinhibition in the human motor cortex is enhanced by synchronous upper limb movements

The phasic modulation of wrist flexor corticomotor disinhibition has previously been demonstrated during the flexion phase of rhythmical passive flexion-extension of the human wrist. Here we ask if rhythmical bimanual flexion-extension movements of the wrists of neurologically intact subjects, modulate inhibitory activity in the motor cortex. In the first experiment intracortical inhibition was assessed when one wrist was passively flexed and extended on its own, with the addition of the opposite limb voluntarily moving synchronously in a mirror symmetric pattern, and also in a near-symmetric asynchronous pattern. Two subsequent experiments investigated firstly the modulation of spinal reflex pathway activity during the same three movement conditions, and secondly the effect of contralateral wrist movement alone on the excitability of corticomotoneuronal pathways to a static test limb. When the wrist flexors of both upper limbs were shortening simultaneously (i.e. synchronously), intracortical inhibition associated with flexor representations was suppressed to a greater extent than when the two muscles were shortening asynchronously. The results of the three experiments indicate that modulation of inhibitory activity was taking place at the cortical level. These findings may have further application in the study of rehabilitation procedures where the effects of simultaneous activation of affected and unaffected upper limbs in hemiparetic patients are to be investigated.     

Interplay of biomechanical and neuromuscular constraints on pattern stability and attentional demands in a bimanual coordination task in human subjects

Recent debate has focused upon the issue of whether general principles and laws of movement coordination may be derived without reference to anatomical, mechanical and physiological mechanisms. It has been proposed that self-generated movement involves the interaction of biomechanical and neuromuscular constraints. Biomechanical constraints are usually considered of as arising from the pendular dimensions of the limb or limb segments whereas neuromuscular constraints are commonly associated with nervous and metabolic control processes. The present study aims to investigate the interplay between these two different constraints on bimanual pattern stability and attentional demands. Five subjects were asked to execute an anti-phase coordination pattern (180 degrees of relative phase), while gradually increasing the frequency of oscillation and changing the rotational inertia of the joysticks. Frequency manipulation was expected to affect the neuromuscular constraints. Inertial manipulation was expected to affect biomechanical constraints. Attentional demands, reflecting the central cost associated with the maintenance of the coordination pattern was assessed using a dual-task paradigm. The results showed that: (1) increasing the oscillation frequency altered both coordination dynamics and attentional demands associated with the maintenance of bimanual coordination patterns; (2) manipulation of rotational inertia of the joysticks also altered pattern stability (standard deviation of relative phase) and coordination dynamics (i.e. the number of phase transition and the before transition), but these alterations were not paralleled by a change in attentional demands.     

Seeing or moving in parallel: the premotor cortex does both during bimanual coordination, while the cerebellum monitors the behavioral instability of symmetric movements

The underlying neural mechanisms of a perceptual bias for in-phase bimanual coordination movements are not well understood. In the present study, we measured brain activity with functional magnetic resonance imaging in healthy subjects during a task, where subjects performed bimanual index finger adduction–abduction movements symmetrically or in parallel with real-time congruent or incongruent visual feedback of the movements. One network, consisting of bilateral superior and middle frontal gyrus and supplementary motor area (SMA), was more active when subjects performed parallel movements, whereas a different network, involving bilateral dorsal premotor cortex (PMd), primary motor cortex, and SMA, was more active when subjects viewed parallel movements while performing either symmetrical or parallel movements. Correlations between behavioral instability and brain activity were present in right lateral cerebellum during the symmetric movements. These findings suggest the presence of different error-monitoring mechanisms for symmetric and parallel movements. The results indicate that separate areas within PMd and SMA are responsible for both perception and performance of ongoing movements and that the cerebellum supports symmetric movements by monitoring deviations from the stable coordination pattern.     

Goal-directed arm movements in absence of visual guidance: evidence for amplitude rather than position control

Summary 1. The control of pointing arm movements in the absence of visual guidance was investigated in unpracticed human subjects. The right arm grasped a lever which restricted the movement of the right index fingertip to a horizontal arc, centered between the axes of eye rotation. A horizontal panel directly above the arm prevented visual feedback of the movement. Visual stimuli were presented in discrete positions just above panel and fingertip. A flag provided visual feedback on fingertip position before each pointing movement (Exp. A and B), or before a movement sequence (Exp. C). 2. When subjects pointed from straight ahead to eccentric stimulus positions (Exp. A), systematic and variable pointing errors were observed; both kinds of errors increased with stimulus eccentricity. When subjects pointed from 30 deg left to stimuli located further right (Exp. B), errors increased with stimulus position to the right. Taken together, these findings suggest that pointing accuracy depends not primarily on stimulus position, but rather on required movement amplitude. 3. When subjects performed sequences of unidirectional movements (Exp. C), systematic and variable errors increased within the sequence. A quantitative analysis revealed that this increase can be best described as an accumulation of successive pointing errors. 4. We conclude that both findings, error increase with amplitude, and accumulation of successive errors, when considered together strongly support the hypothesis that amplitude, rather than final position, is the controlled variable of the investigated movements.     

Neuromuscular and biomechanical factors codetermine the solution to motor redundancy in rhythmic multijoint arm movement

How the CNS deals with the issue of motor redundancy remains a central question for motor control research. Here we investigate the means by which neuromuscular and biomechanical factors interact to resolve motor redundancy in rhythmic multijoint arm movements. We used a two-df motorised robot arm to manipulate the dynamics of rhythmic flexion–extension (FE) and supination–pronation (SP) movements at the elbow-joint complex. Participants were required to produce rhythmic FE and SP movements, either in isolation, or in combination (at the phase relationship of their choice), while we recorded the activity of key bi-functional muscles. When performed in combination, most participants spontaneously produced an in-phase pattern of coordination in which flexion is synchronised with supination. The activity of the Biceps Brachii (BB), the strongest arm muscle which also has the largest moment arms in both flexion and supination was significantly higher for FE and SP performed in combination than in isolation, suggesting optimal exploitation of the mechanical advantage of this muscle. In a separate condition, participants were required to produce a rhythmic SP movement while a rhythmic FE movement was imposed by the motorised robot. Simulations based upon a musculoskeletal model of the arm demonstrated that in this context, the most efficient use of the force–velocity relationship of BB requires that an anti-phase pattern of coordination (flexion synchronized with pronation) be produced. In practice, the participants maintained the in-phase behavior, and BB activity was higher than for SP performed in isolation. This finding suggests that the neural organisation underlying the exploitation of bifunctional muscle properties, in the natural context, constrains the system to maintain the “natural” coordination pattern in an altered dynamic environment, even at the cost of reduced biomechanical efficiency. We suggest an important role for afference from the imposed movement in promoting the “natural” pattern. Practical implications for the emerging field of robot-assisted therapy and rehabilitation are briefly mentioned.