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Bilateral basal ganglia activation associated with sensorimotor adaptation

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Abstract

Sensorimotor adaptation tasks can be classified into two types. When subjects adapt movements to visual feedback perturbations such as in prism lens adaptation, they perform kinematic adaptations. When subjects adapt movements to force field perturbations such as with robotic manipulanda, they perform kinetic adaptations. Neuroimaging studies have shown basal ganglia involvement in kinetic adaptations, but have found little evidence of basal ganglia involvement in kinematic adaptations, despite reports of deficits in patients with diseases of the basal ganglia, such as Parkinson’s and Huntington’s disease, in these. In an effort to resolve such apparent discrepancy, we used FMRI to focus on the first few minutes of practice during kinematic adaptation. Human subjects adapted to visuomotor rotations in the context of a joystick aiming task while lying supine in a 3.0 T MRI scanner. As demonstrated previously, early adaptive processes were associated with BOLD activation in the cerebellum and the sensory and motor cortical regions. A novel finding of this study was bilateral basal ganglia activation. This suggests that, at least for early learning, the neural correlates of kinematic adaptation parallel those of other types of skill learning. We observed activation in the right globus pallidus and putamen, along with the right prefrontal, premotor and parietal cortex, which may support spatial cognitive processes of adaptation. We also observed activation in the left globus pallidus and caudate nucleus, along with the left premotor and supplementary motor cortex, which may support the sensorimotor processes of adaptation. These results are the first to demonstrate a clear involvement of basal ganglia activation in this type of kinematic motor adaptation.

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Acknowledgments

This work was supported by grants from the UM FMRI Center and the UM Rackham faculty grant program, NIH AG024106, and NIH AG08808 (UM Claude D. Pepper OAIC Research Career Development Core). We thank K. Newnham for his expertise during data collection, and J. Ashe, V. Penhune and C. Ojakangas for providing thoughtful comments on earlier drafts of this manuscript.

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Seidler, R.D., Noll, D.C. & Chintalapati, P. Bilateral basal ganglia activation associated with sensorimotor adaptation. Exp Brain Res 175, 544–555 (2006). https://doi.org/10.1007/s00221-006-0571-y

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