Effect of transcranial magnetic stimulation on bimanual movements

Transcranial magnetic stimulation (TMS) of the motor cortex can interrupt voluntary contralateral rhythmic limb movements. Using the method of "resetting index" (RI), our study investigated the TMS effect on different types of bimanual movements. Six normal subjects participated. For unimanual movement, each subject tapped either the right or left index finger at a comfortable rate. For bimanual movement, index fingers of both hands tapped in the same (in-phase) direction or in the opposite (antiphase) direction. TMS was applied to each hemisphere separately at various intensities from 0.5 to 1.5 times motor threshold (MT). TMS interruption of rhythm was quantified by RI. For the unimanual movements, TMS disrupted both contralateral and ipsilateral rhythmic hand movements, although the effect was much less in the ipsilateral hand. For the bimanual in-phase task, TMS could simultaneously reset the rhythmic movements of both hands, but the effect on the contralateral hand was less and the effect on the ipsilateral hand was more compared with the unimanual tasks. Similar effects were seen from right and left hemisphere stimulation. TMS had little effect on the bimanual antiphase task. The equal effect of right and left hemisphere stimulation indicates that neither motor cortex is dominant for simple bimanual in-phase movement. The smaller influence of contralateral stimulation and the greater effect of ipsilateral stimulation during bimanual in-phase movement compared with unimanual movement suggest hemispheric coupling. The antiphase movements were resistant to TMS disruption, and this suggests that control of rhythm differs in the 2 tasks. TMS produced a transient asynchrony of movements on the 2 sides, indicating that both motor cortices might be downstream of the clocking command or that the clocking is a consequence of the 2 hemispheres communicating equally with each other.     

Reaching movements in children: accuracy and reaction time development

The present study was undertaken to follow the development of the capability to produce adult-like fast and precise movements reaching visual targets, during childhood. A two-dimensional reaching task was used. We focussed on pre-planning capabilities, by instructing subjects to produce movements as fast as possible, preventing corrections after initiation of movement. The capability of information processing and accurate motor response production were assessed by measuring reaction time (RT, the time elapsed between target presentation and movement onset), movement time (MT, the time elapsed between movement onset and movement end) and precision of response (correlation of response extent and direction with target distance and direction). One child (male) was tested repeatedly since age 6 until age 9. At age 7, RTs decreased. At age 8, accuracy increased, after a temporary decrease at 7. Both accuracy and RT eventually reached the adult level. MTs were similar to the adult ones right from the beginning and they never changed significantly. The results were confirmed in four groups of five children each, aged 6, 7, 8 and 9, respectively. A control group of five adults was also tested. It is concluded that, between age 6 and 9, children become capable of quickly processing visual target information and producing accurate fast and uncorrected reaching trajectories based upon proprioceptive information only, like those typical of adults, by shortening RTs and improving precision, while maintaining adult-like MTs throughout. The capability of quickly reacting to a target acting as a `Go’ signal (measured by RT) and that of information processing to program an accurate motor trajectory (measured by the precision achieved) appear not to be developmentally linked, the former improving earlier, the latter later.     

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.     

Decoding higher-order motor information from primate non-primary motor cortices.

To investigate the involvement of primate non-primary motor cortices in bimanual sequential movements, we recorded neuronal activity in the supplementary motor area (SMA) and presupplementary motor area (pre-SMA) while an animal was performing bimanual motor tasks that required two sequential arm movements consisting of either pronation or supination of the right or left arms with delay periods. We also recorded electromyograms (EMGs) from the arm while the animal performed the bimanual task to compare muscle and neuronal activity. This paper focuses on the neuronal activity before the onset of sequential movements. We found that the prime-mover forelimb muscles were selectively active when an impending arm movement involved recorded muscles, but was not dependent on whether the arm movements were bimanual or unimanual. In contrast, we found that neurons in the non-primary motor cortices showed different activity depending on whether the forthcoming sequential arm movements were unimanual or bimanual. Our results suggest that neuronal activity in the SMA and pre-SMA reflects higher-order information about arm use before motor execution. By extracting this type of information, we can use it to control prosthetic arms in a more intelligent manner through a brain-machine interface.     

Comparing movement preparation of unimanual,bimanual symmetric,and bimanual asymmetric movements

The goal of this study was to determine the process or processes most likely to be involved in reaction-time costs for spatially cued bimanual reaching. We used reaction time to measure the cost of bimanual symmetric movements compared to unimanual movements (a bimanual symmetric cost) and the cost for bimanual asymmetric movements compared to symmetric movements (a bimanual asymmetric cost). The results showed that reaction times were comparable for all types of movements in simple reaction time; that is, there was neither a bimanual symmetric cost nor an asymmetric cost. Therefore, unimanual, bimanual symmetric, and bimanual asymmetric movements have comparable complexity during response initiation. In choice conditions, there was no bimanual symmetric cost but there was a bimanual asymmetric cost, indicating that the preparation of asymmetric movements is more complex than symmetric movements. This asymmetric cost is likely the result of interference during response programming.     

Resource-demanding versus cost-effective bimanual interaction in the brain

When two hands require different information in bimanual asymmetric movements, interference can occur via callosal connections and ipsilateral corticospinal pathways. This interference could potentially work as a cost-effective measure in symmetric movements, allowing the same information to be commonly available to both hands at once. Using functional magnetic resonance imaging, we investigated supra-additive and sub-additive neural interactions in bimanual movements during the initiation and continuation phases of movement. We compared activity during bimanual asymmetric and symmetric movements with the sum of activity during unimanual right and left finger-tapping. Supra-additive continuation-related activation was found in the right dorsal premotor cortex and left cerebellum (lobule V) during asymmetric movements. In addition, for unimanual movements, the right dorsal premotor cortex and left cerebellum (lobule V) showed significant activation only for left-hand (non-dominant) movements, but not for right-hand movements. These results suggest that resource-demanding interactions in bimanual asymmetric movements are involved in a non-dominant hand motor network that functions to keep non-dominant hand movements stable. We found sub-additive continuation-related activation in the supplementary motor area (SMA), bilateral cerebellum (lobule VI) in symmetric movements, and the SMA in asymmetric movements. This suggests that no extra demands were placed on these areas in bimanual movements despite the conventional notion that they play crucial roles in bimanual coordination. Sub-additive initiation-related activation in the left anterior putamen suggests that symmetric movements place lower demands on motor programming. These findings indicate that, depending on coordination patterns, the neural substrates of bimanual movements either exhibit greater effort to keep non-dominant hand movements stable, or save neural cost by sharing information commonly to both hands.     

Common organization for unimanual and bimanual reach-to-grasp tasks

 In two experiments comparisons between characteristics of performance of a unimanual and a bimanual reach-to-grasp (prehension) task were made on an individual subject basis. The unimanual prehension task used required that the object be grasped by finger and thumb pad opposition, the bimanual task required that the grasp be made by opposing the pads on the two index fingers. Experiment 1 examined adaptation of prehension movements to objects of different size (width) but equal grasp surface area placed at different distances. Experiment 2 examined adaptation of movements to objects of different grasp surface areas. It was found that the aperture and transport components of the two prehension tasks developed over time in very similar fashion in all subjects. Movements were adapted to different task constraints in the same way as has previously been reported in the literature and were very similar in both tasks: maximum aperture increases with increasing object size and occurs later in the movement for larger objects; movement time increases with target distance; time of maximum aperture occurs earlier in the movement for targets with smaller grasp surface areas; movement times are longer for such objects, largely due to increases in the deceleration phase of the movement. These results support the notion that there is an effector independent level of organization that governs the coordination of movements during performance of reaching and grasping tasks. Received: 24 May 1996 / Accepted: 9 December 1996     

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     

Deficit in motor cortical activity for simultaneous bimanual responses

Reaction time (RT) is known to be longer for simultaneous bimanual responses than for unimanual ones. This phenomenon is called "bilateral deficit". To identify the mechanisms subserving the bilateral deficit, brain electrical activity was examined, with a source derivation method, in 12 right-handed subjects, during the preparation and execution periods of a RT task. The responses were either unilateral or bilateral index finger flexion, performed either in a simple RT condition, with 20% catch trials, or in a choice RT condition. A deficit was observed in RT for the bilateral response for the right-index finger movement. In cerebral electrical activities, no evidence of a correlate of a bilateral deficit was found during the preparatory period. Conversely, during the execution period, an EEG correlate of the bilateral deficit was found. For the right hand, the activation of the sensorimotor area directly involved in the voluntary control was weaker for bilateral than for unilateral contralateral responses. The reasons for such a bilateral command weakness are discussed in the context of our RT task. First, the constraint of synchronisation included in the bilateral response might require an interhemispheric information transmission that resulted in a braking effect. Second, given that an ipsilateral inhibition is present in case of choice between the two hands of one particular unimanual response, and given that this ipsilateral inhibition is also present in case of simple unimanual trials, we hypothesise that a mutual transcallosal inhibitory effect also persists in the bilateral response. Electronic Publication     

Dynamical changes in corticospinal excitability during imagery of unimanual and bimanual wrist movements in humans: a transcranial magnetic stimulation study

This study explored the dynamical changes in corticospinal excitability during the imagination of cyclical unimanual and bimanual wrist flexion-extension movements. Transcranial magnetic stimulation was applied over the left motor cortex to evoke motor evoked potentials in the right wrist flexor and extensor muscles. Findings provided evidence for increased reciprocal excitability changes during imagery of symmetrical in-phase movements as compared to asymmetrical (anti-phase) or unimanual movements. This suggests that in-phase movements may reinforce whereas anti-phase movements may reduce the temporal representation of the task in the corticospinal motor networks of the brain.     

Cerebral midline structures in bimanual coordination

In six healthy right-handed volunteers, we compared the cerebral activation pattern related to unimanual right- and left-hand movements and to bimanual in-phase and anti-phase movements using functional magnetic resonance imaging (fMRI). Internally paced unimanual finger-to-thumb opposition movements led to a strong contralateral activation of primary sensorimotor areas in all six subjects. Midline activity was lateralized to the left side during right-hand movements, but to both sides during left-hand movements. Activity patterns of bimanual in-phase movements resembled the combined activity patterns of the two unimanual conditions: right and left hemispheric activations of the primary sensorimotor cortices and predominantly left-sided medial frontal activity. In contrast, during anti-phase movements, we observed a clear increase in activity, in both right and left frontal midline areas and in right hemispheric, mainly dorsolateral premotor areas compared to in-phase movements. These results indicate that frontal midline activity is not specific for bimanual movements per se. It can already be involved during simple unimanual movements but becomes progressively more involved during more complex aspects of movement control. Received: 20 September 1998 / Accepted: 24 February 1999     

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.     

Local field potentials related to bimanual movements in the primary and supplementary motor cortices

We recorded local field potentials (LFP) in primary (MI) and supplementary (SMA) motor areas of rhesus monkey cortex in order to compare movement-evoked potentials (mEP) in bimanual and unimanual movements with single-unit activity recorded concurrently. The mEP was often different during bimanual and unimanual movements (a "bimanual-related" effect), but, unlike the single units, the size of the mEP in both MI and SMA was always greater during bimanual movements than during unimanual movements. This increase primarily reflected an increase in the late positive peak of the mEP, a result that may reflect greater overall cortical activation during bimanual movements. In addition, analysis of the mEP revealed differences between MI and SMA not seen in the single-unit activity. mEP in MI had greater contralateral preference than in SMA. Also, SMA mEP was more correlated to the single-unit activity than in MI. This greater correlation was also more apparent in the late peaks of the mEP than in the early peaks and may reflect a greater influence of recurrent activation in SMA than in MI. Our results further reinforce the idea that unimanual and bimanual movements are represented differently both in MI and in SMA and also show that a complex relationship between spikes of individual neurons and LFP may reflect the different input-output relations of different cortical areas. Electronic Publication     

Context influences on the preparation and execution of reaching movements

The ability of rapidly adapting our motor behaviour in order to face the unpredictable changes in the surrounding environment is fundamental for survival. To achieve such a high level of efficiency our motor system has to assess continuously the context in which it acts, gathering all available information that can be relevant for planning goal-oriented movements. One still-debated aspect of movement organization is the nature and timing of motor planning. While motor plans are often taken to be concerned with the setting of kinematic parameters as a function of perceptual and motor factors, it has been suggested that higher level, cognitive factors may also affect planning. To explore this issue further, we asked 18 right-handed human participants to perform speeded hand-reaching movement toward a visual target in two different experimental settings, a reaction time (RT) paradigm (go-only task) and a countermanding paradigm. In both tasks participants executed the same movements, but in the countermanding task no-stop trials were randomly intermixed with stop trials. In stop trials participants were required to withhold the ongoing movement whenever a stop signal was shown. It is known that the presence of stop trials induces a consistent increase of the RTs of no-stop trials with respect to the RTs of go-only trials. However, nothing is known about a similar effect for movement times (MTs). We found that RTs and MTs exhibit opposing tendencies, so that a decrease in the RT correspond to an increase in the MT and vice versa. This tendency was present in all our participants and significant in 90% of them. Furthermore we found a moderate, but again very consistent, anticorrelation between RTs and MTs on a trial-by-trial base. These findings are consistent with strategic changes in movement programmes for the very same movements under different cognitive contexts, requiring different degrees of feedback-driven control during movement.     

Context influences on the preparation and execution of reaching movements

The ability of rapidly adapting our motor behaviour in order to face the unpredictable changes in the surrounding environment is fundamental for survival. To achieve such a high level of efficiency our motor system has to assess continuously the context in which it acts, gathering all available information that can be relevant for planning goal-oriented movements. One still-debated aspect of movement organization is the nature and timing of motor planning. While motor plans are often taken to be concerned with the setting of kinematic parameters as a function of perceptual and motor factors, it has been suggested that higher level, cognitive factors may also affect planning. To explore this issue further, we asked 18 right-handed human participants to perform speeded hand-reaching movement toward a visual target in two different experimental settings, a reaction time (RT) paradigm (go-only task) and a countermanding paradigm. In both tasks participants executed the same movements, but in the countermanding task no-stop trials were randomly intermixed with stop trials. In stop trials participants were required to withhold the ongoing movement whenever a stop signal was shown. It is known that the presence of stop trials induces a consistent increase of the RTs of no-stop trials with respect to the RTs of go-only trials. However, nothing is known about a similar effect for movement times (MTs). We found that RTs and MTs exhibit opposing tendencies, so that a decrease in the RT correspond to an increase in the MT and vice versa. This tendency was present in all our participants and significant in 90% of them. Furthermore we found a moderate, but again very consistent, anticorrelation between RTs and MTs on a trial-by-trial base. These findings are consistent with strategic changes in movement programmes for the very same movements under different cognitive contexts, requiring different degrees of feedback-driven control during movement.     

Physically coupling two objects in a bimanual task alters kinematics but not end-state comfort

People often grasp objects with an awkward grip to ensure a comfortable hand posture at the end of the movement. This end-state comfort effect is a predominant constraint during unimanual movements. However, during bimanual movements the tendency for both hands to satisfy end-state comfort is affected by factors such as end-orientation congruency and task context. Although bimanual end-state comfort has been examined when the hands manipulate two independent objects, no research has examined end-state comfort when the hands are required to manipulate two physically-coupled objects. In the present experiment, kinematics and grasp behavior during a unimanual and bimanual reaching and placing tasks were examined, when the hands manipulate two physically-connected objects. Forty-five participants were assigned to one of three groups; unimanual, bimanual no-spring (the objects were not physically connected), and bimanual spring (the objects were connected by a spring), and instructed to grasp and place objects in various end-orientations, depending on condition. Physically connecting the objects did not affect end-state comfort prevalence. However, it resulted in decreased interlimb coupling. This finding supports the notion of a flexible constraint hierarchy, in which action goals guide the selection of lower level action features (i.e., hand grip used for grasping), and the particular movements used to accomplish that goal (i.e., interlimb coupling) are controlled throughout the movement.     

Changes in neuronal activity of the monkey precentral cortex during preparation for movement

The aim of this study was to analyze the changes in neuronal activity of the motor cortex associated with preparation for movement. Monkeys were trained to perform a between-hands choice-reaction time (RT) task. They pressed upon two levers with both hands and, after a preparatory period of 1-s duration initiated by a warning tone, they must point at either a left- or right-located target, when illuminated as a response signal, with either the left or right hand. The level of preparation for performing either sided movement was changed by manipulating, across block of trials, the relative probabilities for the left and right hands to point at the corresponding target. When considering behavioral data averaged over daily sessions, it was found that RT significantly decreased as response probability increased, whereas movement time (MT) was not affected. However, large changes in this rule were observed when data collected within a single session were considered. Response probability manipulation was acting on RT alone in 27% of sessions, on MT alone in 19% of sessions, and on both RT and MT in 17% of sessions. Statistically significant trial-by-trial correlations between RT and MT were found; of positive sign for 34% of sessions and of negative sign for 12% of sessions. Electromyographic recordings from the biceps and triceps brachii showed that muscle activity remained stable during the preparatory period, both muscles of the performing arm began to be coactivated about 70-130 ms before the lever release, biceps activation being progressively larger than that of the triceps, and the rising slope of biceps activation was steeper for short than for long RTs. Single-cell recording techniques were used to study the neuronal activity of primary motor cortex during the performance of the task. One hundred and fifteen units in area 4, whose activity was recorded during a whole experimental session, were selected for further analysis. Disregarding 4% of units which did not exhibit any movement-related change in activity, it was found that twenty-one percent of units were related to contralateral movements only, 2% to ipsilateral movements only, and 73% to both sided movements. Among this last subset, 27% of units exhibited reciprocal movement-related changes in activity, the most often an excitation for contralateral movements and an inhibition for ipsilateral movements, and 50% of units exhibited a movement-related change in activity in the same direction for both movements, the most often an excitation.(ABSTRACT TRUNCATED AT 400 WORDS)     

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.     

Simultaneous bimanual dynamics are learned without interference

Dynamic learning in humans has been extensively studied using externally applied force fields to perturb movements of the arm. These studies have focused on unimanual learning in which a force field is applied to only one arm. Here we examine dynamic learning during bimanual movements. Specifically we examine learning of a force field in one arm when the other arm makes movements in a null field or in a force field. For both the dominant and non-dominant arms, the learning (change in performance over the exposure period) was the same regardless of whether the other arm moved in a force field, equivalent either in intrinsic or extrinsic coordinates, or moved in a null field. Moreover there were no significant differences in learning in these bimanual tasks compared to unimanual learning, when one arm experienced a force field and the other arm was at rest. Although the learning was the same, there was an overall increase in error for the non-dominant arm for all bimanual conditions compared to the unimanual condition. This increase in error was the result of bimanual movement alone and was present even in the initial training phase before any forces were introduced. We conclude that, during bimanual movements, the application of a force field to one arm neither interferes with nor facilitates simultaneous learning of a force field applied to the other arm.     

Limited transfer of learning between unimanual and bimanual skills within the same limb

Although a limb's motion appears to be similar across unimanual and bimanual movements, here we demonstrate partial, but not complete, transfer of learning across these behavioral contexts, hidden learning that remains intact (but invisible) until the original context is again encountered, and the ability to associate two conflicting force fields simultaneously, one with each context. These results suggest partial, but not complete, overlap in the learning processes involved in the acquisition of unimanual and bimanual skills.