Impaired motor timing control in specific reading retardation

The temporal organizations of unimanual and coordinated bimanual finger tapping was compared between adolescent normal and retarded readers of above average intelligence. The same subjects were examined for speech articulation during the timed repetition of single syllables and syllable sequences. Retarded readers had substantially greater difficulty on tasks of interlimb coordination than on unimanual tapping and substantially greater difficulty rapidly sequencing syllable strings than repeating single syllables. An experimental manipulation of movement speed for both tasks indicated that the threshold at which movement speed degrades timing precision for coordinated action best characterizes the motor impairment of retarded readers.     

The neural dynamics of timed motor tasks: evidence from a synchronization-continuation paradigm

Distinct processing that integrates an accurate time scale is necessary for optimal motor behaviour. In the present study, corticocortical interactions as determined by EEG coherence were assessed in a synchronization–continuation paradigm during which subjects initially performed tapping movements in synchrony with external cues, followed by internal pacing of the target interval when the metronome was switched off. Unimanual and bimanual tasks were executed, and continuation of tapping was conducted with the same or different effector(s). The data showed an increased degree of mesial–central connectivity in the unpaced as compared to paced performance that was independent of task complexity, pointing to a general intensified demand of temporal processing when external cues are unavailable. When switching temporal information between effectors, coherence increased across the motor network. This increase depended upon preceding task complexity, and was most prominent for interhemispheric connections when performing unimanual tasks following bimanual pacing. Overall the data illustrate that timing of skilled actions can easily be transferred between effectors, although increased neural resources are required to conform to the temporal and motor constraints.     

Intercerebellar coupling contributes to bimanual coordination

Compared to unimanual task execution, simultaneous bimanual tapping tasks are associated with a significantly reduced intertap variability. It has been suggested that this bimanual advantage is based on the integration of timing signals which otherwise control each hand independently. Although its functional and anatomic foundations are poorly understood, functional coupling between cerebellar hemispheres might be behind this process. Because the execution of fast alternating fingertaps increases intertap variability, it is hypothesized that intercerebellar coupling is reduced in such tasks. To shed light on the functional significance of intercerebellar coupling, 14 right-handed subjects performed unimanual right, bimanual simultaneous, and bimanual alternating synchronization tasks with respect to a regular auditory pacing signal. In all conditions, within-hand intertap interval was 500 msec. Continuous neuromagnetic activity, using a 122-channel wholehead neuromagnetometer and surface electromyograms of the first dorsal interosseus muscle of both hands, were recorded. For data analysis, we used the analysis tool Dynamic Imaging of Coherent Sources, which provides a tomographic map of cerebromuscular and cerebrocerebral coherence. Analysis revealed a bilateral cerebello-thalamo-cortical network oscillating at alpha (8-12 Hz) and beta (13-24 Hz) frequencies associated with bimanual synchronization. In line with our hypothesis, coupling between cerebellar hemispheres was restricted to simultaneous task execution. This result implies that intercerebellar coupling is key for the execution of simultaneous bimanual movements. Although the criticality of a specific magneto-encephalography pattern for behavioral changes should be interpreted with caution, data suggest that intercerebellar coupling possibly represents the functional foundation of the bimanual advantage.     

Bimanual coordination: neuromagnetic and behavioral data

It has been suggested that bimanual coordination is associated with stronger activation of the left motor cortex in right-handers. The aim of the present study was to investigate whether left motor cortex dominance constitutes a fundamental feature of bimanual coordination. We investigated neuromagnetic responses while subjects performed a bimanual tapping task using a 122-channel whole-head neuromagnetometer. Three neuromagnetic sources localized in the primary sensorimotor cortex of each hemisphere were found. Sources represent neuromagnetic correlates of the motor command and of somatosensory feedback. Since we found no differences of amplitudes or latencies of corresponding sources of both hemispheres, our data suggest that dominance of the left motor cortex is not a fundamental characteristic for bimanual coordination.     

Timing factors in the coordination of speech movements

Speech movement coordination involves substantial timing adjustments among multiple degrees of muscles and movement freedom. The present investigation examined the kinematic and muscle timing adjustments associated with the production of select speech movements. For oral closing movements, the timing of the upper lip, lower lip, and jaw peak velocities were found to be tightly coupled, apparently reflecting a coordinative strategy. In contrast, oral opening movements demonstrated reduced temporal coupling and inconsistent sequencing across subjects. Overall, it appears that the temporal organization of speech movements varies with the specific movement goals. In order to evaluate the coordinative patterns for oral closing in detail, the temporal adjustments of multiple perioral muscles associated with the systematic closing peak velocity relations were examined. The relative timing of muscle onsets and peak EMG amplitudes was found to be predictably related to the peak velocity timing variations, suggesting that the motor commands are temporally scaled to generate changes in speaking conditions. It was also found that the mechanical properties of the speech articulators influence movement coordination and can be exploited to maximize movement efficiency. The systematic change in muscle timing characteristics for all synergistic muscles apparently reduces the degrees of freedom to control, thereby facilitating the coordination process.     

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.     

Coordination constraints during bimanual versus unimanual performance conditions

Coordinated behaviour is prominent during daily life activities in various combinations and degrees of complexity. Here the influence of coordination constraints upon motor behaviour is evaluated by contrasting two-finger tapping (in-phase and anti-phase) during bimanual and unimanual conditions. Cortical dynamics was assessed by means of EEG coherence in the beta frequency band (13-30 Hz) and included intrahemispheric, interhemispheric and midline connectivity patterns. Results showed that intrahemispheric connectivity varied strongly in the different coordination tasks, with left hemisphere dominance for bimanual and right hand coordination versus right hemisphere dominance for left hand coordination. Interhemispheric connectivity was fairly similar across coordination tasks, except for the bimanual in-phase configuration that comprised the lowest coherence scores. Midline connectivity was equivalent across coordination tasks, with exception of the bimanual anti-phase assignment that was characterized with increased coherence scores. Across connectivity regions, the lowest coherence scores were obtained for bimanual and right hand coordination performed in the in-phase mode, underlining their basic mode of functioning. Furthermore by evaluating the coordination effort, estimated by the discrepancy between the coordination task and the sum of the individual components, an increased processing for intrahemispheric and midline connections was observed, but not for interhemispheric connections, which supports the general significance of interhemispheric communication for voluntary movement. Overall the current findings indicate a dynamic modulation of functional connectivity patterns according to the coordinative context. It suggests that brain regions within a motor network flexibly couple and decouple to implement the processing requirements associated with coordinated behaviour.     

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.     

Evidence in bimanual finger-tapping of an attentional component to stuttering

The performance of right- and left-handed male and female stutters was compared with that of non-stutters on a bimanual coordination task that involved tapping a key twice with one hand for each single tap of a key by the other hand. Right-handed non-stutters performed this 2:1 tapping better when it was the right hand that tapped twice (R2/L1 condition) rather than the left hand (L2/R1 condition), but among left-handers performance was similar under the two conditions. This replicated previous findings of Peters10 that were interpreted as indicating the role of attentional mechanisms in the expression of handedness. The performance of the stutters differed in two major respects. First, overall bimanual tapping rates were significantly slower than those of the non-stutters. Second, right-handed stutters did not show the asymmetry in performance between the R2/L1 and L2/R1 conditions. The results are interpreted within the framework of current neuropsychological research that relates stuttering to anomalous mechanisms of interhemispheric communication.     

Motor control programs and walking.

The question of how the central nervous system coordinates muscle activity is central to an understanding of motor control. The authors argue that motor programs may be considered as a characteristic timing of muscle activations linked to specific kinematic events. In particular, muscle activity occurring during human locomotion can be accounted for by five basic temporal components in a variety of locomotion conditions. Spatiotemporal maps of spinal cord motoneuron activation also show discrete periods of activity. Furthermore, the coordination of locomotion with voluntary tasks is accomplished through a superposition of motor programs or activation timings that are separately associated with each task. As a consequence, the selection of muscle synergies appears to be downstream from the processes that generate activation timings.     

Role of the corpus callosum in bimanual coordination: a comparison of patients with congenital and acquired callosal damage

The objective of the study was to investigate temporal control in patients with congenital as compared to acquired pathology of the corpus callosum during two different bimanual paradigms: (i) a drawer-opening task during which one hand opened a drawer while the other hand reached and grasped a small object, and (ii) rhythmical circling movements that were executed according to the in-phase or antiphase mode. Synchronization values revealed that patients with acquired callosal dysfunction generally showed optimal behaviour during the goal-directed and familiar drawer-opening task but demonstrated strong tendencies towards desynchronization during circling movements, which became most apparent for antiphase coordination. Whereas one patient with callosal agenesis showed a similar performance, the other acallosal patients performed both activities successfully. These observations indicate that patients with congenital absence of the corpus callosum can make use of compensatory mechanisms for allowing temporal synchronization during bimanual movements whereas patients with acquired callosal dysfunction are severely hampered when the task places significant demands on the control processes. The data also underline that the ability of callosal patients to precisely time events in coordinated actions depend on the task constraints.     

Frequency-induced changes in interlimb interactions: increasing manifestations of closed-loop control

In bimanual coordination, interactions between the limbs result in attraction to in-phase and antiphase coordination. Increasing movement frequency leads to decreasing stability of antiphase coordination, often resulting in a transition to the more stable in-phase pattern. It is unknown, however, how this frequency-induced loss of stability is engendered in terms of the interlimb interactions underwriting bimanual coordination. The present study was conducted to help resolve this issue. Using an established method (based on comparison of various unimanual and bimanual tasks involving both passive and active movements), three sources of interlimb interaction were dissociated: (1) integrated timing of feedforward signals, (2) afference-based correction of relative phase errors, and (3) phase entrainment by contralateral afference. Results indicated that phase entrainment strength remained unaffected by frequency and that the stabilizing effects of error correction and integrated timing decreased with increasing frequency. Their contributions, however, reflected an interesting interplay as frequency increased. For moderate frequencies coordinative stability was predominantly secured by integrated timing processes. However, at high frequencies, the stabilization of the antiphase pattern required combined contributions of both integrated timing and error correction. In sum, increasing frequency was found to induce a shift from predominantly open-loop control to more closed-loop control. The results may be accounted for by means of an internal forward model for sensorimotor integration in which the sensory signals are compared to values predicted on the basis of efference copies.     

The oscillatory network of simple repetitive bimanual movements

Bimanual synchronization relies on the precisely coordinated interplay of both hands. It is assumed that during temporal bimanual coordination, timing signals controlling each hand might be integrated. Although a specific role of the cerebellum for this integration process has been suggested, its neural foundations are still poorly understood. Since dynamic interactions between spatially distributed neural activity are reflected in oscillatory neural coupling, the aim of the present study was to characterize the dynamic interplay between participating brain structures. More specifically, the study aimed at investigating whether any evidence for the integration of bilateral cerebellar hemispheres could be found. Seven right-handed subjects synchronized bimanual index finger-taps to a regular pacing signal. We recorded continuous neuromagnetic activity using a 122-channel whole-head neuromagnetometer and surface EMGs of the first dorsal interosseus (FDI) muscle of both hands. Coherence analysis revealed that an oscillatory network coupling at 8-12 Hz subserves task execution. The constituents are bilateral primary sensorimotor and premotor areas, posterior-parietal and primary auditory cortex, thalamus and cerebellum. Coupling occurred at different cortical and subcortical levels within and between both hemispheres. Coupling between primary sensorimotor and premotor areas was observed directly and indirectly via the thalamus. Coupling direction suggests that information was integrated within the left premotor cortex corroborating a specific role of the left premotor cortex for motor control in right-handers. Most importantly, our data indicate strong coupling between both cerebellar hemispheres substantiating the hypothesis that cerebellar signals might be integrated during task execution.     

Cognitive executive function in dystonia.

Dystonia is a movement disorder considered to result from basal ganglia dysfunction. The aim of this study was to investigate the functional significance of frontal hyperactivity demonstrated in dystonia in imaging studies by examining executive function and working memory, in which the prefrontal cortex is known to be involved. We assessed 10 patients with idiopathic dystonia and 12 age- and IQ-matched normal controls. All subjects completed tests of first letter, category, and alternating category word fluency, the Wisconsin Card Sorting Test, the Stroop Colour Word Naming Test, the Missing Digit Test of working memory, a test of random number generation, a test requiring generation of self-ordered random number sequences, the Paced Serial Addition Test, a test of conditional associative learning, and finger tapping and peg insertion under unimanual, bimanual, and dual task conditions. The patients with dystonia did not differ significantly from controls on any measures of executive function or working memory used other than category word fluency and the extent of decline in tapping with one hand under dual task conditions when simultaneously inserting pegs with the other hand. For this small sample, the results suggest that unlike other movement disorders associated with fronto-striatal dysfunction such as Parkinson's disease or Huntington's disease, dystonia was not associated with deficits on the tests of executive function or working memory used. A more detailed investigation of cognitive function in a larger sample of patients is required.     

Differential callosal contributions to bimanual control in young and older adults

Our recent work has shown that older adults are disproportionately impaired at bimanual tasks when the two hands are moving out of phase with each other [Bangert, A. S., Reuter-Lorenz, P. A., Walsh, C. M., Schachter, A. B., & Seidler, R. D. Bimanual coordination and aging: Neurobehavioral implications. Neuropsychologia, 48, 1165-1170, 2010]. Interhemispheric interactions play a key role during such bimanual movements to prevent interference from the opposite hemisphere. Declines in corpus callosum (CC) size and microstructure with advancing age have been well documented, but their contributions to age deficits in bimanual function have not been identified. In the current study, we used structural magnetic resonance and diffusion tensor imaging to investigate age-related changes in the relationships between callosal macrostructure, microstructure, and motor performance on tapping tasks requiring differing degrees of interhemispheric interaction. We found that older adults demonstrated disproportionately poorer performance on out-of-phase bimanual control, replicating our previous results. In addition, older adults had smaller anterior CC size and poorer white matter integrity in the callosal midbody than their younger counterparts. Surprisingly, larger CC size and better integrity of callosal microstructure in regions connecting sensorimotor cortices were associated with poorer motor performance on tasks requiring high levels of interhemispheric interaction in young adults. Conversely, in older adults, better performance on these tasks was associated with larger size and better CC microstructure integrity within the same callosal regions. These findings implicate age-related declines in callosal size and integrity as a key contributor to bimanual control deficits. Further, the differential age-related involvement of transcallosal pathways reported here raises new questions about the role of the CC in bimanual control.     

Automaticity and attention in Huntington's disease: When two hands are not better than one

People with Huntington's disease (HD) commonly report difficulty carrying out two everyday tasks simultaneously. This difficulty, confirmed by experimental studies, is typically ascribed to impaired attention. Yet, dual-task problems extend to relatively simple tasks, such as walking and talking, which would ordinarily be considered relatively undemanding of attention. The study tests the hypothesis that in HD there is a deficit in the ability to automatise task performance. Thus, simple tasks, which place minimal demands on conscious attention in healthy controls, make disproportionately high demands on attentional resources in HD. We examined the performance of HD patients and healthy controls on a simple, paced finger-tapping task, comparing single-task (tapping with one hand) and dual-task (tapping with both hands simultaneously) performance. For HD patients, bimanual tapping increased the task demands: there was greater variability in tapping rate and patients reported that the ‘dual-task’ condition was more difficult. The opposite pattern was observed for controls. Variability in tapping performance in HD was highly correlated with performance on cognitive tasks that have the potential to be automatised but not with performance on tasks that are more demanding of executive control, suggesting a common substrate for cognitive and motor automaticity. The data support the hypothesis that HD patients are impaired in their capacity for automisation, and suggest that impaired automaticity may be one source of attentional deficits in HD. The findings have implications for the interpretation of ‘high level’ deficits in attention and executive function previously reported in HD.     

Poor penmanship in children correlates with abnormal rhythmic tapping: a broad functional temporal impairment

Timing is crucial for proficient motor tasks; temporal impairments may lead to dysfunctional motor activities. Although much research has been dedicated to the study of movement timing, clinical examination often overlooks temporal impairment of motor activity. The authors hypothesize that some children have a global temporal impairment leading to dysfunctional motor skills. This article checks whether temporal abnormalities detected on a simple tapping task correlate with temporal dysfunction during complex motor skills such as handwriting. Twenty-three school-aged children, 8-14 years (11.1 +/- 1.3 years), underwent tests to assess finger tapping and cursive handwriting. Handwriting samples were rated by experienced teachers. Children with abnormal tapping had lower handwriting rating scores. Temporal features were similar in both tasks; variability on the tapping test correlated with handwriting variability. Temporal variability was not significantly higher for children with poor penmanship as a whole but rather specific to the subgroup of children with a tapping abnormality. Poor penmanship could be attributed in certain children to global temporal impairment reflected as variable finger tapping and handwriting. Evaluation of dysfunctional motor performance should include temporal aspects, and further studies are needed to better delineate and address treatment of "dysrhythmia."     

Timing of rhythmic movements in patients with cerebellar degeneration

A distinction in temporal performance has been identified between two classes of rhythmic movements: those requiring explicit timing of salient events marking successive cycles, i.e., event timing, and continuous movements in which timing is hypothesized to be emergent. Converging evidence in support of this distinction is reviewed, including neuropsychological studies showing that individuals with cerebellar damage are selectively impaired on tasks requiring event timing (e.g., tapping). Recent behavioral evidence in neurologically healthy individuals suggests that for continuous movements (e.g., circle drawing), the initial cycle is marked by a transformation from event to emergent timing, allowing the participant to match their movement rate to an externally defined cycle duration. We report a new experiment in which individuals with cerebellar ataxia produced rhythmic tapping or circle drawing movements. Participants were either paced by a metronome or unpaced. Ataxics showed a disproportionate increase in temporal variability during tapping compared to circle drawing, although they were more variable than controls on both tasks. However, two predictions of the transformation hypothesis were not confirmed. First, the ataxics did not show a selective impairment on circle drawing during the initial cycles, a phase when we hypothesized event timing would be required to establish the movement rate. Second, the metronome did not increase variability of the performance of the ataxics. Taken together, these results provide further evidence that the integrity of the cerebellum is especially important for event timing, although our attempt to specify the relationship between event and emergent timing was not successful.     

Optical imaging of intrinsic signals in somatosensory cortex

The experiments address the problem of bimanual coordination in a familiar task of everyday life. A goal-directed drawer-pulling task, with asymmetrical assignments among hands, was analyzed with the objective to detect discrete kinematic events ('anchors') that potentially could serve in proper goal synchronization. The left hand reached out for the drawer and opened it while the right hand performed a prehension movement to pick up a peg from the drawer. The task was smoothly performed, independently of vision. Typically, trajectories and velocity profiles of the leading pull-hand were more stereotypical than the more variable ones of the pick-hand. The pull-hand had a large velocity peak during reaching, followed by a small peak during pulling. Velocity profiles of the pick-hand were not bell-shaped and exhibited one or two broad waves, often with an irregular and probing evolution. Velocity profiles of both hands were aligned with the first or the second velocity peak of the leading pull-hand. In the majority of cases, temporal associations of events in the kinematics of the two limbs could thus be identified, which could serve to synchronize the hands at the goal. The nearly straight biphasic reach-and-pull trajectory of the leading hand contrasted with the more curved trajectory of the right pick-hand whereas, in the same unimanual action, the latter trajectories were quasi-rectilinear. Changing constraints (no vision, cutaneous anesthesia of pulling fingers) could change the coordination pattern. We argue that bimanual coordination relies on two interacting mechanisms: (1) feedforward control on the basis of sensorimotor memory; (2) temporal adjustments during the evolving bimanual synergy. Multiple strategies, imposed by the leading pull-hand, appeared to be responsible for feedback-induced corrections in the pick-hand and were found to contribute to the goal-invariance and to the principle of motor equivalence.     

Gait profiles as indicators of domain-specific impairments in executive control across neurodevelopmental disorders

In neurodevelopmental disorders, unique profiles of executive control and attention appear to co-occur with poor motor coordination. However, less is known about how syndrome-specific cognitive profiles interact with motor control and impact behavioural outcomes in neurodevelopmental disorders such as Williams syndrome (WS) and Down syndrome (DS). Here we aimed to examine the extent to which specific components of executive function interact with gait control when performing cognitive dual-tasks (verbal fluency, digit span) in WS and DS. Spatiotemporal gait characteristics and intra-individual variability of gait were assessed in individuals with WS who were matched on spatial ability to individuals with DS, and chronologically age (CA) matched controls. During the concurrent verbal fluency task, the WS group had greater dual-task costs on spatiotemporal gait parameters and variability than CA controls. Conversely, individuals with DS had selective gait interference during the concurrent digit span task when compared to CA controls, but only under increased demands on cognitive control where there was greater variability in step timing in DS. The interrelationships between cognitive-motor interference and behavioural measures of executive functioning appeared to differentiate between WS and DS, and emphasise the importance of task modality in unpacking the executive control profile in these neurodevelopmental disorders. These findings support the notion that associated cerebellar-cortico abnormalities may produce quite distinct profiles of executive control across cognitive and motor domains that impact on behavioural outcomes in neurodevelopmental disorders.