Neural Representation of Orientation Relative to Gravity in the Macaque Cerebellum

Abstract

A fundamental challenge for maintaining spatial orientation and interacting with the world is knowledge of our orientation relative to gravity, i.e., head tilt. Sensing gravity is complicated because of Einstein's equivalence principle, in which gravitational and translational accelerations are physically indistinguishable. Theory has proposed that this ambiguity is solved by tracking head tilt through multisensory integration. Here we identify a group of Purkinje cells in the caudal cerebellar vermis with responses that reflect an estimate of head tilt. These tilt-selective cells are complementary to translation-selective Purkinje cells, such that their population activities sum to the net gravitoinertial acceleration encoded by the otolith organs, as predicted by theory. These findings reflect the remarkable ability of the cerebellum for neural computation and provide quantitative evidence for a neural representation of gravity, whose calculation relies on long-postulated theoretical concepts such as internal models and Bayesian priors.