Encoding of action by the Purkinje cells of the cerebellum

Abstract

SummaryExecution of accurate eye movements depends critically on the cerebellum1,2,3, suggesting that Purkinje cells (P-cells) may predict motion of the eye. Yet, this encoding has remained a long-standing puzzle: P-cells show little consistent modulation with respect to saccade amplitude4,5 or direction4, and critically, their discharge lasts longer than duration of a saccade6,7. Here, we analyzed P-cell discharge in the oculomotor vermis of behaving monkeys8,9 and found neurons that increased or decreased their activity during saccades. We estimated the combined effect of these two populations via their projections on the caudal fastigial nucleus (cFN) and uncovered a simple-spike population response that precisely predicted the real-time motion of the eye. When we organized the P-cells according to each cell's complex-spike directional tuning, the simple-spike population response predicted both the real-time speed and direction of saccade multiplicatively via a gain-field. This suggests that the cerebellum predicts the real-time motion of the eye during saccades via the combined inputs of P-cells onto individual nucleus neurons. A gain-field encoding of simple spikes emerges if the P-cells that project onto a nucleus neuron are not selected at random, but share a common complex-spike property.

The same oculomotor vermal Purkinje cells encode the different kinematics of saccades and of smooth pursuit eye movements

“…However, one might think that the strong influence of eye position in the case of saccades is at odds with a previous report27 emphasizing a reflection of eye speed and direction in the population discharge of OMV PCs. However, closer consideration indicates that there is actually no contradiction whatsoever.…”

Individual Differences in Motor Noise and Adaptation Rate Are Optimally Related

“…Central to the forward model is the cerebellar Purkinje cell, which responds to selected sensory (Chabrol et al, 2015) and motor (Kelly and Strick, 2003) parallel fiber input with a firing pattern reflecting kinematic properties of upcoming movements (Pasalar et al, 2006; Herzfeld et al, 2015). When Purkinje cell predictions of the upcoming kinematic properties are inaccurate, activity of neurons in the cerebellar nuclei is proportional to the prediction error.…”

The Cerebellum: Adaptive Prediction for Movement and Cognition

“…This idea, supported by a substantial literature involving various tasks and species, centers on the idea that the cerebellum receives a copy of the motor command [45–47] and, in combination with exteroceptive and proprioceptive sensory inputs, generates a representation of the expected sensory consequences of that command [45, 48–50]. An alternative and potentially complementary theory argues that the cerebellum contributes to the generation of motor commands, functioning as an inverse model [51–53].…”

“…Hence, the Purkinje cell simple spike activity could be viewed as constituting the sensory prediction [45, 46, 63] (although it may also contribute to the motor command), while the climbing fiber activity resulting in Purkinje cell complex spikes provides a representation of sensory prediction errors [64–66], driving cerebellar learning. It should be noted that, although this model has been highly influential in theories of cerebellar-based learning, there remains considerable debate over the functional role of the climbing fiber signals and their interaction with simple spike activity [50, 64, 67]. Furthermore, recent physiological data in mice and rats suggest cerebellar modules vary in the firing rate of simple spike activity and exhibit plasticity tuned to different time intervals between parallel and climbing fiber inputs [20, 21, 68].…”