Abstract
We investigated simple directional hand movements based on different degrees of muscle co-activity, at behavioral and cerebral level in healthy subjects and Parkinson's disease (PD) patients. We compared “singular” movements, dominated by the activity of one agonist muscle, to “composite” movements, requiring conjoint activity of multiple muscles, in a center-out (right hand) step-tracking task. Behavioral parameters were obtained by EMG and kinematic recordings. fMRI was used to investigate differences in underlying brain activations between PD patients (N = 12) and healthy (age-matched) subjects (N = 18). In healthy subjects, composite movements recruited the striatum and cortical areas comprising bilaterally the supplementary motor area and premotor cortex, contralateral medial prefrontal cortex, primary motor cortex, primary visual cortex, and ipsilateral superior parietal cortex. Contrarily, the ipsilateral cerebellum was more involved in singular movements. This striking dichotomy between striatal and cortical recruitment vs. cerebellar involvement was considered to reflect the complementary roles of these areas in motor control, in which the basal ganglia are involved in movement selection and the cerebellum in movement optimization. Compared to healthy subjects, PD patients showed decreased activation of the striatum and cortical areas in composite movement, while performing worse at behavioral level. This implies that PD patients are especially impaired on tasks requiring highly tuned muscle co-activity. Singular movement, on the other hand, was characterized by a combination of increased activation of the ipsilateral parietal cortex and left cerebellum. As singular movement performance was only slightly compromised, we interpret this as a reflection of increased visuospatial processing, possibly as a compensational mechanism.
Highlights
The direction of voluntary hand movement along the wrist originates from cerebrally encoded vectors, without a direct link to specific muscles to effectuate their contraction
We primarily looked for effects in the basal ganglia (BG)/thalamus, premotor cortex (PMC), supplementary motor area (SMA), parietal cortex and cerebellum
One healthy subject was excluded from the behavioral part of the study, due to a technical problem that occurred while recording the kinematic data
Summary
The direction of voluntary hand movement along the wrist originates from cerebrally encoded vectors, without a direct link to specific muscles to effectuate their contraction. The basal ganglia (BG) are known to modify the cortically generated motor plan by selecting appropriate muscles and inhibiting undesired motor activity (Alexander et al, 1986; Mink, 1996; Middleton and Strick, 2000; Rubchinsky et al, 2003; de Jong and Paans, 2007) In studies addressing these aspects of direction tuning in motor control, center-out step-tracking tasks (Hoffman and Strick, 1999) are commonly used. Given the association between pathophysiological BG changes and characteristic movement impairments in Parkinson’s disease (PD) (DeLong and Wichmann, 2009), we included PD patients, expecting to find reduced BG activity during movements requiring highly tuned muscle co-activity, when compared to healthy subjects This concept finds support from the observation that muscle tuning is impaired in PD as patients show insufficient inhibition of antagonist muscles, which causes co-contraction of agonist and antagonist muscles (Meunier et al, 2000). To gain insight in the impaired selection of highly tuned muscle co-activity in PD patients, the here employed center-out step-tracking task enabled the comparison of movements executed with different degrees of muscle tuning between PD patients and healthy subjects both at behavioral level, using kinematic and electromyography (EMG) parameters, and at the cerebral level by using functional magnetic resonance imaging (fMRI)
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