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

Abstract

AbstractIndividuals with cerebellar deficits exhibit a broad range of motor impairments when performing voluntary movements. However, the sequence of events leading to these impairments and the distinction between primary and compensatory processes remain unclear. We addressed this question by reversibly blocking cerebellar outflow in monkeys performing planar center-out movements. We found that a reduced hand velocity observed when blocking cerebellar outflow during reaching movements is due to a decrease in muscle torque and a spatially tuned reduction in velocity, particularly pronounced during movements involving inter-joint interactions. The time course of these two processes was examined using the sequence of trials of movements to the same target when blocking cerebellar outflow. We found that during multi-joint reaching movements, the reduced velocity was driven by an acute deficit superimposed on a gradually emergent strategic slowing aimed to minimize passive inter-joint interactions. Finally, the reduction in velocity could not explain the increased motor noise observed during a cerebellar block, which manifested as decomposed and variable trajectories. Our results suggest that loss of cerebellar signals leads to motor impairments through insufficient muscle torques and altered motor control strategy to compensate for the impaired control of limb dynamics. However, impaired feedforward control also increases motor noise, which cannot be strategically eliminated.Significance StatementOur study examined the impact of cerebellar dysfunction on movement control by reversibly blocking the cerebellar output in monkeys. During a cerebellar block, reaching movements initially slowed due to an acute deficit in generating muscle torque. Beyond this primary deficit, there appeared to be a secondary, strategic slowing down 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. These findings highlight the role of the cerebellar in movement control and delineate the processes following cerebellar dysfunction that culminate in a broad range of motor impairments.