Simple spike dynamics of Purkinje cells in the macaque vestibulo-cerebellum reflect sensory prediction error

Abstract

Theories of cerebellar functions posit that the cerebellum implements forward models for online correction of motor actions and sensory estimation. As an example of such computations, a forward model compensates for a sensory ambiguity where the peripheral otolith organs in the inner ear sense both head tilts and translations. Here we exploit the response dynamics of two functionally-coupled Purkinje cell types in the caudal vermis to understand their role in this computation. We find that one population encodes tilt velocity, whereas the other, translation-selective, population encodes linear acceleration. Using a dynamical model, we further show that these signals likely represent sensory prediction error for the on-line updating of tilt and translation estimates. These properties also reveal the need for temporal integration between the tilt-selective velocity and translation-selective acceleration population signals. We show that a simple model incorporating a biologically plausible short time constant can mediate the required temporal integration.