Bimanual motor coordination controlled by cooperative interactions in intrinsic and extrinsic coordinates

Although strong motor coordination in intrinsic muscle coordinates has frequently been reported for bimanual movements, coordination in extrinsic visual coordinates is also crucial in various bimanual tasks. To explore the bimanual coordination mechanisms in terms of the frame of reference, here we characterized implicit bilateral interactions in visuomotor tasks. Visual perturbations (finger‐cursor gain change) were applied while participants performed a rhythmic tracking task with both index fingers under an in‐phase or anti‐phase relationship in extrinsic coordinates. When they corrected the right finger's amplitude, the left finger's amplitude unintentionally also changed [motor interference (MI)], despite the instruction to keep its amplitude constant. Notably, we observed two specificities: one was large MI and low relative‐phase variability (PV) under the intrinsic in‐phase condition, and the other was large MI and high PV under the extrinsic in‐phase condition. Additionally, using a multiple‐interaction model, we successfully decomposed MI into intrinsic components caused by motor correction and extrinsic components caused by visual‐cursor mismatch of the right finger's movements. This analysis revealed that the central nervous system facilitates MI by combining intrinsic and extrinsic components in the condition with in‐phases in both intrinsic and extrinsic coordinates, and that under‐additivity of the effects is explained by the brain's preference for the intrinsic interaction over extrinsic interaction. In contrast, the PV was significantly correlated with the intrinsic component, suggesting that the intrinsic interaction dominantly contributed to bimanual movement stabilization. The inconsistent features of MI and PV suggest that the central nervous system regulates multiple levels of bilateral interactions for various bimanual tasks.     

Impaired visuo-motor sequence learning in Developmental Coordination Disorder

The defining feature of Developmental Coordination Disorder (DCD) is the marked impairment in the development of motor coordination (DSM-IV-TR, American Psychiatric Association, 2000). In the current study, we focused on one core aspect of motor coordination: learning to correctly sequence movements. We investigated the procedural, visuo-motor sequence learning abilities of 18 children with DCD and 20 matched typically developing (TD) children, by means of the serial reaction time (SRT) task. Reaction time measurements yielded two important findings. Overall, DCD children demonstrated general learning of visuo-motor task demands comparable to that of TD children but failed to learn the visuo-motor sequence. Interestingly, a sequence recall test, administered after the SRT task, indicated some awareness of the repeating sequence pattern. This suggests that the sequence learning problems of DCD children might be located at the stage of motor planning rather than sequence acquisition.     

Unilateral versus bilateral tasks in early asymmetric Parkinson's disease: differential effects on bradykinesia.

Patients with Parkinson's disease (PD) have an impaired ability to perform two different simultaneous bimanual tasks. The differential effects of unilateral versus bilateral identical tasks on the bradykinesia scores of the more and less affected limbs in PD have not been examined. Twenty-seven patients with early and asymmetric PD underwent blinded, videotaped assessment, independently for each limb, using the bradykinesia items of the Unified Parkinson's Disease Rating Part III, Motor subscale (mUPDRS) and a Modified Bradykinesia Rating Scale (MBRS), which assessed amplitude, speed, and rhythm of movements. We found that the score for finger tapping in mUPDRS and MBRS, the score of amplitude of finger tapping in MBRS, and the lateralized scores of mUPDRS (sum of Items 23 to 25) of the most affected side significantly improved during the bimanual task. The improvement was associated with longer duration of illness, higher total scores in mUPDRS, and higher lateralized bradykinesia scores of the most affected side. There was a simultaneous deterioration of the lateralized bradykinesia scores in MBRS (sum of Items 23 to 25) and Item 25 of mUPDRS (rapid alternating movements) of the least affected side in bimanual tasks. In conclusion, identical bimanual tasks facilitate movement of the most affected side in early asymmetric PD at the cost of motor degradation in the least affected side. This observation also highlights the need to perform tasks of bradykinesia in one limb at a time for best accuracy.     

Unimanual and Bimanual Simultaneous Fingertapping in Schoolchildren: Developmental Aspects and Hand Preference-related Asymmetries

Computerised analysis of finger tapping was performed in 233 normal 5- to 12-year-old children whose hand preference was assessed with six demonstration actions. Performance with both hands became more rapid with age when tapping unimanually or simultaneously in phase with two hands as quickly as possible. There were no differences between the sexes. Performance with both hands also acquired more tapping regularity with age during unimanual tapping, whereas only the left hand did so during bimanual tapping. There was no age effect on the dexterity (speed) difference between unimanually tapping hands, nor on the relative time lag and the degree of synchrony between the hands in bimanual tapping. The degree of synchrony, however, becomes more stable in older children. The more righthanded children are, the faster the right hand is in unimanual tapping, and the more the right hand is ahead of the left hand during bimanual tapping. However, there is a right shift for both of these variables which makes them poor predictors of hand preference. These results suggest that there is a strong bias towards the right hand in complete righthanders as well as-to a lesser extent-in all others, which might be connected to the leading role of the left hemisphere for the performance aspects of hand motor function under study.     

An examination of writing pauses in the handwriting of children with Developmental Coordination Disorder

Difficulties with handwriting are reported as one of the main reasons for the referral of children with Developmental Coordination Disorder (DCD) to healthcare professionals. In a recent study we found that children with DCD produced less text than their typically developing (TD) peers and paused for 60% of a free-writing task. However, little is known about the nature of the pausing; whether they are long pauses possibly due to higher level processes of text generation or fatigue, or shorter pauses related to the movements between letters. This gap in the knowledge-base creates barriers to understanding the handwriting difficulties in children with DCD. The aim of this study was to characterise the pauses observed in the handwriting of English children with and without DCD. Twenty-eight 8–14 year-old children with a diagnosis of DCD participated in the study, with 28 TD age and gender matched controls. Participants completed the 10 min free-writing task from the Detailed Assessment of Speed of Handwriting (DASH) on a digitising writing tablet. The total overall percentage of pausing during the task was categorised into four pause time-frames, each derived from the literature on writing (250 ms to 2 s; 2–4 s; 4–10 s and >10 s). In addition, the location of the pauses was coded (within word/between word) to examine where the breakdown in the writing process occurred. The results indicated that the main group difference was driven by more pauses above 10 s in the DCD group. In addition, the DCD group paused more within words compared to TD peers, indicating a lack of automaticity in their handwriting. These findings may support the provision of additional time for children with DCD in written examinations. More importantly, they emphasise the need for intervention in children with DCD to promote the acquisition of efficient handwriting skill.     

Concurrent performance of motor tasks and processing capacity in patients with schizophrenia

Any task is carried out more successfully if we allocate undivided attention to it, but as demands on attentional capacity increase-for example, in concurrent or dual task conditions-performance on attended tasks becomes more impaired. Patients with schizophrenia show impaired performance on tasks requiring high levels of attentional capacity. This study examines performance of 11 patients with schizophrenia and 13 normal controls on two motor tasks (placing pegs in a pegboard and repetitive index finger tapping) under unimanual, bimanual, and dual task conditions. The patients with schizophrenia placed fewer pegs and had reduced tapping speed in unimanual and bimanual conditions. However, the decrement in bimanual performance as a percentage of unimanual performance was not significantly different for the patients and controls on either the pegboard or tapping tasks. By contrast, under dual task conditions, the performance of the patients with schizophrenia in peg placement actually improved relative to the unimanual pegboard task, whereas tapping performance deteriorated compared with the unimanual tapping, a decrement that was significantly greater for the patients. Thus the improvement in the visually guided pegboard task was at the expense of the repetitive tapping task. These results are discussed in terms of an impairment of self initiated movement with general sparing of externally triggered movements in schizophrenia and the role of frontostriatal loops in this process.     

Physical fitness in children with Developmental Coordination Disorder: Measurement matters

Children with Developmental Coordination Disorder (DCD) experience considerable difficulties coordinating and controlling their body movements during functional motor tasks. Thus, it is not surprising that children with DCD do not perform well on tests of physical fitness. The aim of this study was to determine whether deficits in motor coordination influence the ability of children with DCD to perform adequately on physical fitness tests. A case–control study design was used to compare the performance of children with DCD (n = 70, 36 boys, mean age = 8y 1mo) and Typically Developing (TD) children (n = 70, 35 boys, mean age = 7y 9mo) on measures of isometric strength (hand-held dynamometry), functional strength, i.e. explosive power and muscular endurance (Functional Strength Measurement), aerobic capacity (20 m Shuttle Run Test) and anaerobic muscle capacity, i.e. muscle power (Muscle Power Sprint Test). Results show that children with DCD were able to generate similar isometric forces compared to TD children in isometric break tests, but were significantly weaker in three-point grip strength. Performance on functional strength items requiring more isolated explosive movement of the upper extremities, showed no significant difference between groups while items requiring muscle endurance (repetitions in 30 s) and items requiring whole body explosive movement were all significantly different. Aerobic capacity was lower for children with DCD whereas anaerobic performance during the sprint test was not. Our findings suggest that poor physical fitness performance in children with DCD may be partly due to poor timing and coordination of repetitive movements.     

Performance on unimanual and bimanual tapping tasks by patients with lesions of the frontal or temporal lobe

The performance of 151 patients with unilateral excisions from either the frontal or the temporal cortex and 60 normal subjects was examined on three motor tasks: (1) simple unimanual tapping; (2) spatially ordered unimanual tapping; and (3) bimanual tapping in which the movements of the two hands were out-of-phase. All patient groups were impaired with both hands on spatially ordered unimanual tapping. In contrast, only those patients with either left or right frontal-lobe lesions performed poorly on the bimanual tapping task. Our findings demonstrate that the frontal cortex plays a critical role in the co-ordination of arm and hand movements, particularly when different movements have to be performed simultaneously.     

Deficits of visuospatial attention with reflexive orienting induced by eye-gazed cues in children with developmental coordination disorder in the lower extremities: An event-related potential study

The present study aims to investigate and compare the behavioral performance and event-related potentials (ERPs) measures in children with developmental coordination disorder (DCD) and typically developing (TD) children when performing the visuospatial attention task with reflexive orienting. Thirty children with DCD and 30 TD children were recruited and presented with central eye-gazed cues. The children needed to detect and respond to laterally presented reaction signals preceded by centrally presented non-predictive directional and non-directional eye-gazed cues, which directed them to attend covertly to the right or left field location, or straight ahead, via stepping on pedals with their bilateral lower limbs, while brain ERPs were concurrently recorded. The behavioral data showed that children with DCD responded slowly and exhibited a deficit in inhibitory control capacity as compared to TD children. In terms of electrophysiological characteristics, children with DCD showed distinct modulatory effects upon longer N2 and P3 latencies, smaller P3 amplitude, an elongated interval between N2 and the motor response (N2 latency-RT), and small areas on Contingent Negative Variation (CNV). The behavioral and ERP data suggest that children with DCD could have deficits in the ventral attention network and the mechanisms on the inhibitory control difficulty, when performing such a task, could be a slower response inhibitory process and stimulus classification speed, less ability in interhemispheric and cognitive-to-motor transfer speed, and less mature abilities with regard to anticipatorily executive and motor preparatory processes.     

Involvement of area MT in bimanual finger movements in left-handers: an fMRI study

The ease with which humans are able to perform symmetric movements of both hands has traditionally been attributed to the preference of the motor system to activate homologous muscles. Recently, we have shown in right-handers, however, that bimanual index finger adduction and abduction movements in incongruous hand orientations (one palm down/other up) preferentially engaged parietal perception-associated brain areas. Here, we used functional magnetic resonance imaging to investigate the influence of hand orientation in left-handers on cerebral activation during bimanual index finger movements. Performance in incongruous orientation of either hand yielded activations involving right and left motor cortex, supplementary motor area in right superior frontal gyrus (SMA and pre-SMA), bilateral premotor cortex, prefrontal cortex, bilateral somatosensory cortex and anterior parietal cortex along the intraparietal sulcus. In addition, the occipito-temporal cortex corresponding to human area MT (hMT) in either hemisphere was activated in relation to bimanual index finger movements in the incongruous hand orientation as compared with the same movements in the congruous hand orientation or with simply viewing the pacing stimuli. Comparison with the same movement condition in right-handed subjects from a former study support these hMT activations exclusively for left-handed subjects. These results suggest that left-handers use visual motion imagery in guiding incongruous bimanual finger movements.     

Unimanual and bimanual simultaneous fingertapping in schoolchildren: developmental aspects and hand preference-related asymmetries

Computerised analysis of finger tapping was performed in 233 normal 5- to 12-year-old children whose hand preference was assessed with six demonstration actions. Performance with both hands became more rapid with age when tapping unimanually or simultaneously in phase with two hands as quickly as possible. There were no differences between the sexes. Performance with both hands also acquired more tapping regularity with age during unimanual tapping, whereas only the left hand did so during bimanual tapping. There was no age effect on the dexterity (speed) difference between unimanually tapping hands, nor on the relative time lag and the degree of synchrony between the hands in bimanual tapping. The degree of synchrony, however, becomes more stable in older children. The more righthanded children are, the faster the right hand is in unimanual tapping, and the more the right hand is ahead of the left hand during bimanual tapping. However, there is a right shift for both of these variables which makes them poor predictors of hand preference. These results suggest that there is a strong bias towards the right hand in complete righthanders as well as-to a lesser extent-in all others, which might be connected to the leading role of the left hemisphere for the performance aspects of hand motor function under study.     

Brain activation associated with motor skill practice in children with developmental coordination disorder: an fMRI study

Children with developmental coordination disorder (DCD) have difficulty in learning new motor skills. At present, it is not known whether these children employ a different set of brain regions than typically developing (TD) children during skilled motor practice. Using functional magnetic resonance imaging, we mapped brain activity associated with skilled motor practice of a trail-tracing task in 7 children with DCD and 7 age-matched controls (aged 8-12 years). We indexed change in motor performance as a reduction in tracing error from early practice to retention. Children with DCD showed less blood-oxygen-level-dependent signal as compared to TD children in a network of brain regions associated with skilled motor practice: bilateral inferior parietal lobules (Brodmann Area (BA) 40), right lingual gyrus (BA 18), right middle frontal gyrus (BA 9), left fusiform gyrus (BA 37), right cerebellar crus I, left cerebellar lobule VI, and left cerebellar lobule IX. While no statistically significant differences were detected, effect size testing revealed that children with DCD demonstrated poorer tracing accuracy than TD children at retention (d = 0.48). Our results suggest that, compared to TD peers, children with DCD demonstrate under-activation in cerebellar-parietal and cerebellar-prefrontal networks and in brain regions associated with visual-spatial learning. These data suggest a neurobiological correlation with impaired learning of motor skills in children with DCD, which will need to be confirmed with a larger sample.     

Lateralized interference effects of concurrent verbal tasks on sequential finger tapping

Twenty-four right-handed subjects concurrently performed both a sequential finger tapping task and a verbal task with or without visual guidance. The concurrent verbal tasks consisted of shadowing with vocalization and of memorizing without vocalization. The result showed that (1) both verbal tasks interfered with right hand tapping but not with left hand tapping, (2) lateralized interference was stronger in the shadowing than in the memorizing condition, and (3) performance did not differ under the visual and the non-visual guidance conditions. These data suggest that non-vocalized verbal tasks interfere with concurrent motor performance by the right hand, and that this lateralized interference effect is weaker than the effect produced by vocalized verbal tasks.     

Evidence of interhemispheric transmission in laterality effects

The study was aimed at testing various models that can explain visual lateral asymmetries due to hemispheric specialization. In Experiments 1-3 the subjects had to perform a lateralized "go-no go" discrimination of words (primary task) either alone or in association with secondary tasks that interfered with the processing of the left hemisphere (ordered tapping) or the right hemisphere (finger flexion). In Experiment 4 the primary task was one of lateralized "go-no go" discrimination of faces while the secondary tasks were again those of ordered tapping and finger flexion. The results showed that in the case of word discrimination the advantage in speed of response in favour of the right visual field/left hemisphere (RVF/LH), which was observed for the primary task alone, did not change when the secondary task was added. This held true irrespective of whether the secondary task loaded the left or right hemisphere. The advantage for the left visual field/right hemisphere (LVF/RH) observed for face discrimination alone, disappeared when the secondary task interfered with the processing of the right hemisphere and did not change when the secondary task concerned the left hemisphere. It was concluded that each hemisphere is able to elaborate in parallel the incoming information, but, in normal conditions, interhemispheric transmission is responsible for the lateral asymmetries in perception (conditional interhemispheric transmission model).     

The Two-Arm Coordination Test: Maturation of Bimanual Coordination in Typically Developing Children and Deficits in Children with Unilateral Cerebral Palsy

ABSTRACT

Background: Tools to assess bimanual coordination are scant. We aimed to: 1) provide normative data of maturation of bimanual coordination in tipically developing (TD) children measured by the Two Arm Coordination Test (TACT), and 2) validate the TACT as an instrument to specifically discriminate impairment of bimanual coordination in children with unilateral cerebral palsy (UCP). Procedure: Cross-sectional observational study. 252 TD children and 26 children with UCP performed 8 trials of TACT (following a star pattern with a pointer steered by coordinated movements of both arms). Number of errors and time were combined in a performance index of motor learning.Results: In TD children, bimanual coordination improved with age (F(7,244)=36.888, p<.001). Children with UCP had a poorer bimanual coordination than TD children (all t>24.25, all p<.01). TACT scores were correlated moderately to manual dexterity and manual ability (all r>-.452, all p<.039), showing the capacity of the TACT to provide information on different aspects of hand function. Conclusion: TACT is a valid instrument to assess bimanual coordination.     

Intermanual coordination in relation to handedness, familial sinistrality and lateral preferences

Intermanual coordination assessed by alternating finger tapping and finger-tapping asymmetry were investigated in 105 healthy right- and 105 left-handers and related to handedness, familial sinistrality and lateral preferences (in hand-clasping, arm-folding and eyedness). Compared to right-handers, left-handers with less pronounced left-hand preferences (Subgroup B) showed higher values in intermanual coordination and lower values in finger-tapping asymmetry. Moreover, familial sinistrality and eyedness interacted with handedness effects. While in right-handers intermanual coordination was significantly higher in subjects with dominant left eye, in left-handers of the Subgroup B it was somewhat higher in those with dominant right eye. Higher values in intermanual coordination and reduced asymmetry in finger tapping may be associated with a greater bihemispheric control and better performance in fast bimanual movements.     

Developmental trends in right hemispheric participation in reading

Behavioral laterality tasks assessed the differential processing efficiencies of the cerebral hemispheres in younger and older reading-age children. Lateralized lexical decision task findings supported a "direct access" model of hemispheric processing for the younger children whereas the older children demonstrated a "callosal relay" pattern. A dual-task with oral and silent reading indicated that the right hand was significantly more disrupted than the left during unimanual finger tapping. The findings suggest that although the left hemisphere's involvement during reading is developmentally stable, the involvement of the right hemisphere appears to change dynamically as reading experience increases.     

Cortical activations in primary and secondary motor areas for complex bimanual movements in professional pianists

Hemodynamic responses were measured applying functional magnetic resonance imaging in two professional piano players and two carefully matched non-musician control subjects during the performance of self-paced bimanual and unimanual tapping tasks. The bimanual tasks were chosen because they resemble typical movements pianists have to generate during piano exercises. The results showed that the primary and secondary motor areas (M1, SMA, pre-SMA, and CMA) were considerably activated to a much lesser degree in professional pianists than in non-musicians. This difference was strongest for the pre-SMA and CMA, where professional pianists showed very little activation. The results suggest that the long lasting extensive hand skill training of the pianists leads to greater efficiency which is reflected in a smaller number of active neurons needed to perform given finger movements. This in turn enlarges the possible control capacity for a wide range of movements because more movements, or more 'degrees of freedom', are controllable.     

A Modified Finger Lift Test Reveals an Asymmetry of Motor Overflow in Adults

Abstract

A method of eliciting motor overflow in neurologically intact adults is reported. A weight was placed on either the middle or ring finger of the left or right hand, and the subject was instructed to lift that finger. Involuntary finger lifts of the contralateral hand were recorded. There were 32 right-handers per experiment. In Experiments I and II, the amount of weight placed on the subject's finger was in proportion to body weight, whereas in Experiment HI, it was in proportion to each finger's strength. Across experiments, motor overflow was more prevalent when the left, rather than the right, hand was weighted. This shows that the asymmetry in motor overflow previously reported in children and brain-damaged adults also occurs in healthy adults, and that this movement asymmetry is not an artifact of the relative weakness of the left hand in right-handed individuals.     

A pianist's recovery from stroke

OBJECTIVE: To determine alternative neural pathways for restitution of piano playing after right hemispheric infarction causing left arm and hand paralysis. DESIGN: Case report testing coordinated bimanual skills using structured motor skills tests and neuroimaging. SETTING: A professional pianist sustained a lacunar infarction in the posterior limb of his right internal capsule, which resulted in left hemiparesis with immobilized left-hand and -finger movements persisting for 13 weeks. After 6 months, he had recovered bimanual coordinated piano skills by "ignoring" his left hand while concentrating or discussing subjects other than music while playing. PATIENT: A 63-year-old, male professional pianist. INTERVENTION: Detailed neurological examination including computed cranial tomography, functional magnetic resonance imaging, and positron emission tomography. RESULTS: Functional magnetic resonance imaging activation patterns correlated with rapid movements of fingers in each hand separately and together demonstrating that subcortical and cerebellar pathways were activated during skilled motor function of his left hand. Contralateral cerebral and cerebellar activation occurred with both left- and right-hand movements. During tapping of the left fingers, there was bilateral cerebellar, parietal, and left premotor strip and left thalamic activation. CONCLUSION: Patterns of activation relate to task performance and they are not similar to subjects engaged in simpler tasks such as finger opposition.