Selective semicircular canal inactivation and three-dimensional eye movement recordings have been used to investigate the spatial organization of vestibular signals in the vestibulo-ocular reflex (VOR) of rhesus monkeys. In animals with one pair of semicircular canals inactivated, afferent activity no longer codes all spatial components of head angular velocity. if it were the activation pattern of semicircular canal afferents alone that determines VOR slow phase eye velocity, the head velocity components along the sensitivity vectors of the remaining intact semicircular canals would determine the orientation of slow phase eye velocity. Thus, angular head velocity and slow phase eye velocity would not necessarily always align. Alternatively, if vestibulo-ocular signals coded absolute angular head motion in space based on both semicircular canal and otolith afferent information, one might expect a spatial transformation of the encoded head angular velocity signals such that slow phase eye velocity and angular head velocity continue to spatially align. Examination of the VOR at different frequencies between 0.01 Hz and 1 Hz revealed a frequency-specific spatial organization of vestibulo-ocular signals. Mid and high frequency vestibulo-ocular responses were determined exclusively by the orientation of the sensitivity vectors of the remaining intact semicircular canals. In contrasts, low frequency vestibulo-ocular responses were largely determined by the orientation of the head relative to gravity. These low frequency responses after selective semicircular canal inactivation could be predicted and simulated by a simple model where semicircular canal signals are spatially transformed from a head-fixed to a space-fixed (inertial) representation of angular head velocity. These findings suggest that low frequency vestibulo-ocular responses are dominated by inertial vestibular signals that detect absolute head motion in space based on both semicircular canal and otolith afferent information. Inertial vestibular signals are likely to contribute to head control and motor coordination of gaze, head and body posture.