Behavior of eye-movement-related cells in the vestibular nuclei during combined rotational and translational stimuli.

1. Secondary position-vestibular-pause (PVP) neurons in the vestibuloocular reflex (VOR) pathway of adult rhesus monkeys were studied during combined semicircular canal and otolith stimulation. The head was rotated at 0.5 Hz with the axis of rotation centered between the otolith organs (on-axis, ON) and with the axis of rotation 23 cm in front of the otoliths (off-axis, OFF). Both conditions were tested with two different vergence angles by the use of 14-cm (near target, NT) and 100-cm (far target, FT) targets. 2. The tangential translational stimulus to the otoliths in the OFF trials should result in a compensatory eye movement that is opposite in direction to that resulting from the angular stimulus to the canals. The otolith stimulus should be great enough to reverse the eye movement response in the NT OFF trials according to geometric calculations. This reversal in eye movement direction occurred as expected although the latency of the reversal (70 ms) was somewhat greater than expected and the magnitude of the reversal was less than predicted solely on the basis of geometric considerations. 3. The responses of the PVP neurons were corrected for eye position sensitivity to investigate the head movement response components. The amplitude of the response in 22 of 24 PVP cells was reduced in the NT OFF condition compared with the FT OFF condition. This difference was not sufficient in itself to explain the observed reversal in eye movement response. 4. The average sensitivities of the neurons to rotation during the FT and NT ON trials were 1.38 and 1.41 spikes.s-1.deg-1.s-1, respectively. This is too small an increase to account for the increase in the angular VOR gain with near targets (approximately 25%); therefore cells other than PVP neurons must be responsible. 5. The average sensitivities of the PVP neurons to translational accelerations obtained from the FT and NT OFF trials were 305 and 484 spikes.s-1.g-1, respectively, which is higher than most otolith afferent sensitivities reported for 0.5-Hz stimuli in the literature. The otolith component is modified by ocular convergence (59% increase in sensitivity), but this increase is too small to account for the change in the translational VOR gain between the two conditions. 6. Although recordings were only obtained from seven eye-head-velocity cells, the results indicate that these neurons may provide the additional signals not present in the PVP cells. These neurons exhibited large differences between ON and OFF rotations and were found to substantially increase their modulation during the NT conditions compared with that observed during the FT conditions.