Our long term goal is to construct a unifying framework that explains the roles of the basal ganglia and the cerebellum in control of saccades and reaching. We suggest that a fundamental assumption regarding control of movements, the idea that variability is mostly because of noise, is incorrect. We show that there is systematic variability in the motor commands that initiate a movement to a target, and propose that this variability is a reflection of a systematic reduction in the internal value that the brain associates with a repeating stimulus. We hypothesize that this internal value is computed in the striatum. If this variability was uncompensated, that is, if movements like saccades were """"""""open loop"""""""", then the variability would affect saccade endpoints. In healthy people, however, saccade endpoints are immune to this variability. We suggest that this is because control of movements is strongly dependent on internal models through the cerebellum, monitoring the outgoing motor commands and effectively """"""""steering"""""""" to compensate for variability in the outgoing motor command that would lead to unacceptable inaccuracy, i.e., dysmetria. The compensation is effective only if this internal model is calibrated, which links the problem of control with adaptation. We propose a single principle of control and adaptation for both the saccadic and reaching systems: each is supported by a fast adaptive system with poor retention, and a slow adaptive system with strong retention. Expected costs and rewards of a movement are evaluated by the basal ganglia, resulting in an internal value that affects the motor commands that initiate the movement. As the motor commands are generated, the cerebellum monitors them and predicts their sensory consequences, producing adjustments that """"""""steer"""""""" the movement to the goal. We propose that adaptation is faster in the mechanism that steers the movement (cerebellum for both reaching and saccades) than the mechanism that initiates the movement (motor cortex for reaching, superior colliculus for saccades).
Our hypothesis is a new, coherent theory of how various brain structures like the basal ganglia and the cerebellum contribute to control of voluntary movements like saccades and reaching. While cerebellar patients have been consistently impaired in motor learning, our hypothesis presents a potential solution to how rehabilitation may proceed in these patients to help their recovery. The role of basal ganglia in control of movements has remained a deep puzzle. Our hypothesized link between this structure and the internal value of action may help early diagnosis of diseases of the basal ganglia through experiments that quantify changes in trajectories of the eyes and the arm in response to changes in value of the stimulus that affords these movements.
| Reppert, Thomas R; Lempert, Karolina M; Glimcher, Paul W et al. (2015) Modulation of Saccade Vigor during Value-Based Decision Making. J Neurosci 35:15369-78 |
| Herzfeld, David J; Pastor, Damien; Haith, Adrian M et al. (2014) Contributions of the cerebellum and the motor cortex to acquisition and retention of motor memories. Neuroimage 98:147-58 |
| Haith, Adrian M; Reppert, Thomas R; Shadmehr, Reza (2012) Evidence for hyperbolic temporal discounting of reward in control of movements. J Neurosci 32:11727-36 |
| Ahmadi-Pajouh, Mohammad Ali; Towhidkhah, Farzad; Shadmehr, Reza (2012) Preparing to reach: selecting an adaptive long-latency feedback controller. J Neurosci 32:9537-45 |
| Marko, Mollie K; Haith, Adrian M; Harran, Michelle D et al. (2012) Sensitivity to prediction error in reach adaptation. J Neurophysiol 108:1752-63 |
| Izawa, Jun; Pekny, Sarah E; Marko, Mollie K et al. (2012) Motor learning relies on integrated sensory inputs in ADHD, but over-selectively on proprioception in autism spectrum conditions. Autism Res 5:124-36 |
| Xu-Wilson, Minnan; Tian, Jing; Shadmehr, Reza et al. (2011) TMS perturbs saccade trajectories and unmasks an internal feedback controller for saccades. J Neurosci 31:11537-46 |
| Izawa, Jun; Shadmehr, Reza (2011) Learning from sensory and reward prediction errors during motor adaptation. PLoS Comput Biol 7:e1002012 |
| Pekny, Sarah E; Criscimagna-Hemminger, Sarah E; Shadmehr, Reza (2011) Protection and expression of human motor memories. J Neurosci 31:13829-39 |
| Orban de Xivry, Jean-Jacques; Criscimagna-Hemminger, Sarah E; Shadmehr, Reza (2011) Contributions of the motor cortex to adaptive control of reaching depend on the perturbation schedule. Cereb Cortex 21:1475-84 |
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