Abstract
Goal-directed movements are predictive and multimodal in nature, especially for moving targets. For instance, during a reaching movement for a moving target, humans need to predict both motion of the target and movement of the limb. Recent computational studies show that the cerebellum predicts current and future states of the body and its environment using internal forward models. Sensory feedback signals from the periphery have delays in reaching the central nervous system, ranging between tens to hundreds of milliseconds. It is well known in engineering that feedback control based on time-delayed inputs can result in oscillatory and often unstable movements. In contrast, the brain predicts a current state from a previous state using forward models. This predictive mechanism most likely underpins stable and dexterous control of reaching movements. Although the cerebro-cerebellum has long been suggested as loci of various forward models, few methods are available to evaluate accuracy of the forward models in patients with cerebellar ataxia. Recently, we developed a non-invasive method to analyze receipt of motor commands in terms of movement kinematics for the wrist joint (Br/Kr ratio). In the present study, we have identified two components (F1 and F2) of the smooth pursuit movement. We found that the two components were in different control modes with different Br/Kr ratios. The major F1 component in a lower frequency range encodes both velocity and position of the moving target (higher Br/Kr ratio) to synchronize movement of the wrist joint with motion of the target in a predictive manner. The minor F2 component in a higher frequency range is biased to position control in order to generate intermittent small step-wise movements. In cerebellar patients, the F1 component shows a selective decrease in the Br/Kr ratio, which is correlated with decrease in accuracy of the pursuit movement. We conclude that the Br/Kr ratio of the F1 component provides a unique parameter to evaluate accuracy of the predictive control. We also discuss the pathophysiological and clinical implications for clinical ataxiology.
Highlights
Goal-directed movements are predictive in nature, especially for moving targets in the environment of daily life
We propose that our new method provides a unique tool to evaluate accuracy of the predictive control in patients with cerebellar ataxia
We examined the relationship between the Br/Kr ratio of the F1 component and accuracy of the pursuit movement (i.e., F1 error, see section “Data Analysis”)
Summary
Goal-directed movements are predictive in nature, especially for moving targets in the environment of daily life. Recent computational studies posit a mechanism that predicts current and future states of the body and its environments by integrating an estimate of previous state and efference copies of motor signals, the computation known as an internal forward model (Wolpert et al, 1995; Miall and Wolpert, 1996; Davidson and Wolpert, 2005). Our group demonstrated that current outputs from the cerebellum (firing rates of dentate cells) contained predictive information about future inputs to the cerebellum (firing rates of mossy fibers), thereby providing a strong support to the forward-model hypothesis of the cerebellum (Tanaka et al, 2019). The computation of a forward model contributes to predictive control in the presence of considerable delays in sensory feedback (Desmurget and Grafton, 2000)
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