The parietoinsular vestibular cortex (PIVC) is a large area in the lateral sulcus with neurons that respond to vestibular stimulation. Here we compare the properties of PIVC cells with those of neurons in brain stem, cerebellum, and thalamus. Most PIVC cells modulated during both translational and rotational head motion. Translation acceleration gains showed a modest decrease as stimulus frequency increased, with a steeper slope than that reported previously for thalamic and cerebellar nuclei neurons. Response dynamics during yaw rotation were similar to those reported for vestibular neurons in brain stem and thalamus: velocity gains were relatively flat through the mid-frequency range, increased at high frequencies, and decreased at low frequencies. Tilt dynamics were more variable: PIVC neurons responsive only to rotation had gains that decreased with increased frequency, whereas neurons responsive during both translation and rotation (convergent neurons) actually increased their modulation magnitude at high frequencies. Using combinations of translation and tilt, most PIVC neurons were better correlated with translational motion; only 14% were better correlated with net acceleration. Thus, although yaw rotation responses in PIVC appear little processed compared with other central vestibular neurons, translation and tilt responses suggest a further processing of linear acceleration signals in thalamocortical circuits.