Trial-to-trial Adaptation: Parsing out the Roles of Cerebellum and BG in Predictive Motor Timing

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Authors

LUNGU Ovidiu V. BAREŠ Martin LIU Tao GOMEZ Christopher M. CECHOVA Ivica ASHE James

Year of publication 2016
Type Article in Periodical
Magazine / Source Journal of Cognitive Neuroscience
MU Faculty or unit

Faculty of Medicine

Citation
Doi http://dx.doi.org/10.1162/jocn_a_00943
Field Neurology, neurosurgery, neurosciences
Keywords BASAL-GANGLIA; RESPONSE-INHIBITION; PARKINSONS-DISEASE; SENSORY PREDICTION; FUNCTIONAL MRI; NEURAL BASIS; TIME; FUTURE; CORTEX; ATAXIA
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Description We previously demonstrated that predictive motor timing (i.e., timing requiring visuomotor coordination in anticipation of a future event, such as catching or batting a ball) is impaired in patients with spinocerebellar ataxia (SCA) types 6 and 8 relative to healthy controls. Specifically, SCA patients had difficulties postponing their motor response while estimating the target kinematics. This behavioral difference relied on the activation of both cerebellum and striatum in healthy controls, but not in cerebellar patients, despite both groups activating certain parts of cerebellum during the task. However, the role of these two key structures in the dynamic adaptation of the motor timing to target kinematic properties remained unexplored. In the current paper, we analyzed these data with the aim of characterizing the trial-by-trial changes in brain activation. We found that in healthy controls alone, and in comparison with SCA patients, the activation in bilateral striatum was exclusively associated with past successes and that in the left putamen, with maintaining a successful performance across successive trials. In healthy controls, relative to SCA patients, a larger network was involved in maintaining a successful trial-by-trial strategy; this included cerebellum and fronto-parieto-temporo-occipital regions that are typically part of attentional network and action monitoring. Cerebellum was also part of a network of regions activated when healthy participants postponed their motor response from one trial to the next; SCA patients showed reduced activation relative to healthy controls in both cerebellum and striatum in the same contrast. These findings support the idea that cerebellum and striatum play complementary roles in the trial-by-trial adaptation in predictive motor timing. In addition to expanding our knowledge of brain structures involved in time processing, our results have implications for the understanding of BG disorders, such as Parkinson disease where feedback processing or reward learning is affected.
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