Disentangling acute motor deficits and adaptive responses evoked by the loss of cerebellar output

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Abstract

Cerebellar patients exhibit a broad range of impairments when performing voluntary movements. However, the sequence of events leading to these deficits and the distinction between primary and compensatory processes remain unclear. We addressed this question by reversibly blocking cerebellar outflow in monkeys performing a planar reaching task. We found that the reduced hand velocity observed under cerebellar block is driven by a combination of a general decrease in muscle torque and a spatially tuned reduction in velocity, particularly pronounced in movements involving inter-joint interactions. The time course of these two processes was examined using repeated movements to the same target under cerebellar block. We found that the reduced velocity was driven by an acute onset of weakness superimposed on a gradually emergent strategy aimed to minimize passive inter-joint interactions. Finally, although the reduced velocity affected movements to all targets, it could not explain the enhanced motor noise observed under cerebellar block, which manifested as decomposed and variable trajectories. Our results suggest that cerebellar deficits lead to motor impairments through a loss of muscle strength and altered motor control strategy to compensate for the impaired control of limb dynamics. However, the loss of feedforward control also leads to increased motor noise, which cannot be strategically eliminated.

Significance Statement

Our study examined the impact of cerebellar dysfunction on motor control by reversibly blocking the cerebellar output in monkeys. Under cerebellar block, movements initially slowed due to acute-onset muscle weakness. Beyond this primary deficit, there was a secondary, seemingly strategic, slowing of movements aimed at mitigating inter-joint interactions associated with rapid, ballistic movements. Finally, during the cerebellar block we observed movement variability increased independently of the reduced velocity, likely reflecting errors in movement planning. Taken together, these findings highlight the role of cerebellar information in motor control and delineate the sequence of processes following cerebellar dysfunction that culminate in a broad range of motor impairments.

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