Does cerebellar cortex function as a forward internal model for motor control?

Abstract

Motor control theorists have postulated that to produce rapid, finely tuned movements, a component of the control circuitry must bypass long sensory feedback delays by providing an estimate of the consequences resulting from a motor command. This control element, termed a forward internal model, receives an efferent copy of the motor command and information about the current state in order to predict the future state (i.e. kinematic variables like position, velocity) of the limb. Previous psychophysical, imaging, and patient case studies suggest that the cerebellum is a possible location for implementation of an internal model. However, very few electrophysiological studies have investigated whether the firing discharge from cerebellar neurons is consistent with the output of a forward internal model. To specifically evaluate the simple spike firing from Purkinje cells in lobules IV-VI, we trained rhesus macaques to perform different hand movement tasks using a 2 joint robotic manipulandum. Two electrophysiology experiments tested several aspects of a forward internal model. First, we hypothesize that Purkinje cell simple spike firing predicts future hand kinematics, even when the task is highly unpredictable. Second, the encoding is invariant, so that the model output can generalize to other tasks. A third hypothesis is that the simple spike discharge will show evidence of learning when animals adapt to a predictable mechanical perturbation, as expected from a forward internal model. Experimental results found many theoretical components of a forward internal model present in the Purkinje cell simple spike discharge. Simple spikes encode both feedforward and feedback representations of movement kinematics, with position and velocity signals explaining the most firing variability. These representations supply the predictive kinematic signals used downstream and the feedback information potentially used locally to construct predictions, calculate errors, and update the model. Many Purkinje cells exhibit dual encoding for a single kinematic parameter, so that these separate feedforward and feedback mechanisms may take place within individual cells. For most cells, model coefficients generated from random tracking data accurately estimate simple spike firing in either circular tracking or center-out reach. Adaptation to a predictable perturbation initiates steady, progressive changes in the parameter sensitivity (βs) of both the feedforward and feedback signals. The timing sensitivity (τ) also demonstrates significant shifts, with time encoding in the simple spikes often changing sign during adaptation (e.g. feedback to feedforward). Population analyses suggest that large changes in parameter sensitivity first occur in the feedback signals, then transfer to the feedforward representations. This may reflect use of the simple spike feedback to update model predictions. These results conclude that kinematic encoding from the cerebellar cortex uses a forward internal model that can generalize between tasks, but is also highly plastic and adaptable.