Ground-truth encoding of self-motion in the primate cerebellar nodulus and uvula

Abstract Accurate internal estimates of self-motion and orientation relative to gravity are fundamental for stabilizing gaze, controlling posture, and navigating through dynamic environments. Prevailing theories propose that the cerebellar nodulus and uvula (NU) employ internal models to suppress sensory input arising from predictable, self-generated motion. However, this assumption has never been directly tested. Here, we recorded NU Purkinje cell activity in rhesus monkeys during active and passive head movements. Neurons responsive to passive translations remained equally active during self-generated movements, encoding net head motion in space irrespective of its source. When motor commands were issued but head motion was blocked, Purkinje cell activity remained unchanged—demonstrating a lack of efference copy integration. During active tilts, NU neurons encoded both dynamic motion and static orientation relative to gravity. These findings challenge the internal model hypothesis and establish the NU as a ground-truth, context-invariant estimator of self-motion, supporting stable behavior in dynamic environments.