The role of the basal ganglia in bimanual coordination

Nuclear Magnetic Resonance Center, Massachusetts General Hospital and Harvard Medical School, Charlestown, MA 02129, USA.
Brain Research (Impact Factor: 2.83). 07/2007; 1151(1):62-73. DOI: 10.1016/j.brainres.2007.01.142
Source: PubMed

ABSTRACT The functional anatomical role of the basal ganglia in bimanual coordination is unknown. Utilizing functional MRI (fMRI) at 3 T, we analyzed brain activity during three different typing tasks. The first task consisted of typing with parallel finger movements (moving left to right with four fingers on both hands). The second task was mirror movements (moving little finger to index finger on both hands), and the third task compared a resting condition with right-handed unimanual typing (moving little finger to index finger). Task dependent BOLD activity in the supplementary motor area (SMA) and dorsolateral premotor areas was observed. In addition, activation patterns were present in the cerebellar vermis during bimanual coordination tasks, with greater activation in the parallel than in the mirror condition. Finally, we also identified activity in the putamen during the tasks described above. Interestingly, putaminal activity was greatest during the period of motor task initiation, and activity during this period was greatest in the parallel condition. Our results suggest a critical role of the basal ganglia in the neural control of bimanual coordination.

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    • "Despite the importance of upper extremity motor function, the impact of providing cues to improve upper extremity performance of PD patients has not been examined systematically. Neuroanatomical (Kraft et al., 2007; Wu, Wang, Hallet, Li, & Chan, 2010) and animal (Kermadi, Liu, Tempini, Calciati, & Rouiller, 1998) studies have indicated that the basal ganglia contribute to supplementary motor area (SMA) function and bimanual coordination. Only a few studies have examined the influence of auditory cues on bimanual timing and coordination of the upper limbs. "
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    ABSTRACT: The present study investigated performance of unimanual and bimanual anti-phase and in-phase upper limb line drawing using three different types of cues. Fifteen Parkinson's disease (PD) patients, 15 elderly, and 15 young adults drew lines away from and towards their body on a tabletop every 1000 ms for 30 s under three different cueing conditions: (1) verbal ('up', 'down'); (2) auditory (high tone, low tone); (3) visual (target line switched from top to bottom). PD patients had larger and more variable amplitudes which may be related to the finding that they also produced more curvilinear movements than young and elderly adults. Consistent with previous research, when compared to the elderly and young adult group PD patients produced a mean relative phase which deviated more from the instructed coordination modes and they showed larger variability of relative phase in bimanual coordination, especially in anti-phase conditions. For all groups, auditory and verbal cues resulted in lower coefficient of variance of cycle time, lower variability of amplitude and lower variability of relative phase than visual cues. The benefit of auditory cues may be related to the timing nature of the task or factors related to the auditory cues (e.g., reduced attentional demands, more kinesthetic focus).
    Human movement science 12/2010; 30(4):770-82. DOI:10.1016/j.humov.2010.08.018 · 2.03 Impact Factor
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    • "2404 | Brain 2010: 133; 2394–2409 T. Wu et al. decreased in patients with Parkinson's disease compared with controls during the performance of bimanual movements (Fig. 3). It has been suggested that the basal ganglia may be crucial in the neural control of bimanual coordination and may be specifically involved in the initiation phase of bimanual movements (Cardoso de Oliveira, 2002; Kraft et al., 2007). Thus, it can certainly be possible that the damaged function of the basal ganglia may impair the ability of patients with Parkinson's disease to perform bimanual tasks. "
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    ABSTRACT: Patients with Parkinson's disease have great difficulty in performing bimanual movements; this problem is more obvious when they perform bimanual anti-phase movements. The underlying mechanism of this problem remains unclear. In the current study, we used functional magnetic resonance imaging to study the bimanual coordination associated changes of brain activity and inter-regional interactions in Parkinson's disease. Subjects were asked to perform right-handed, bimanual in-phase and bimanual anti-phase movements. After practice, normal subjects performed all tasks correctly. Patients with Parkinson's disease performed in-phase movements correctly. However, some patients still made infrequent errors during anti-phase movements; they tended to revert to in-phase movement. Functional magnetic resonance imaging results showed that the supplementary motor area was more activated during anti-phase movement than in-phase movement in controls, but not in patients. In performing anti-phase movements, patients with Parkinson's disease showed less activity in the basal ganglia and supplementary motor area, and had more activation in the primary motor cortex, premotor cortex, inferior frontal gyrus, precuneus and cerebellum compared with normal subjects. The basal ganglia and dorsolateral prefrontal cortex were less connected with the supplementary motor area, whereas the primary motor cortex, parietal cortex, precuneus and cerebellum were more strongly connected with the supplementary motor area in patients with Parkinson's disease than in controls. Our findings suggest that dysfunction of the supplementary motor area and basal ganglia, abnormal interactions of brain networks and disrupted attentional networks are probably important reasons contributing to the difficulty of the patients in performing bimanual anti-phase movements. The patients require more brain activity and stronger connectivity in some brain regions to compensate for dysfunction of the supplementary motor area and basal ganglia in order to perform bimanual movements correctly.
    Brain 08/2010; 133(Pt 8):2394-409. DOI:10.1093/brain/awq151 · 10.23 Impact Factor
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    • "We searched for regions showing greater continuationrelated activation during BA than BS movements. Consistent with previous studies (Sadato et al. 1997; Stephan et al. 1999; Immisch et al. 2001; Meyer-Lindenberg et al. 2002; Aramaki et al. 2006; Kraft et al. 2007), the SMA-proper, bilateral PMd, bilateral parietal, bilateral insula, bilateral globus pallidus, bilateral cerebellum and vermis were more activated in BA than BS movements (P < 0.05 corrected at the cluster level with a height threshold of P < 0.001, masked inclusively with the BA > rest image; Fig. 2a). On the other hand, we found no areas exhibiting signiWcantly greater continuation-related activation during BS than BA movements. "
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    ABSTRACT: 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.
    Experimental Brain Research 04/2010; 203(2):407-18. DOI:10.1007/s00221-010-2244-0 · 2.17 Impact Factor
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