Functional links between neuronal activity and perception are studied by examining trial-by-trial correlations (choice probabilities) between neural responses and perceptual decisions. We addressed fundamental issues regarding the nature and origin of choice probabilities by recording from subcortical (brainstem and cerebellar) neurons in rhesus monkeys during a vestibular heading discrimination task. Subcortical neurons showed robust choice probabilities that exceeded those seen in cortex (area MSTd) under identical conditions. The greater choice probabilities of subcortical neurons could be predicted by a stronger dependence of correlated noise on tuning similarity, as revealed by population decoding. Significant choice probabilities were observed almost exclusively for neurons that responded selectively to translation, whereas neurons that represented net gravito-inertial acceleration did not show choice probabilities. These findings suggest that the emergence of choice probabilities in the vestibular system depends on a critical signal transformation that occurs in subcortical pathways to distinguish translation from orientation relative to gravity.