1. The single-unit activity of neurons in the vestibular nucleus, the prepositus nucleus, and the abducens nucleus, whose activity was primarily related to horizontal eye movements, was recorded in alert squirrel monkeys that were trained to track a small visual target by generating smooth pursuit eye movements and to cancel their horizontal vestibuloocular reflex (VOR) by fixating a head stationary target. 2. The spiking behavior of each cell was recorded during 1) spontaneous eye movements, 2) horizontal smooth pursuit of a target that was moved sinusoidally +/- 20 degrees/s at 0.5 Hz, 3) horizontal VOR evoked by 0.5-Hz sinusoidal turntable rotations +/- 40 degrees/s (VORs), and 4) voluntary cancellation of the VOR by fixation of a head-stationary target during 0.5-Hz sinusoidal turntable rotation at +/- 40 degrees/s (VORCs). The responses of most (28/42) of the units were recorded during unpredictable 100-ms steps in head acceleration (400 degrees/s2) that were generated while the monkey was fixating a target light. The acceleration steps were generated either when the monkey was stationary or when the turntable was already rotating (VORt trials), and the monkey was canceling its VOR (VORCt trials). 3. The firing behavior of all 12 of the abducens neurons recorded was closely related to horizontal eye position and eye velocity during all of the behavioral paradigms used, although there was a small but significant increase in the eye position sensitivity of many of these units when the eye was moving (smooth pursuit) versus when the eye was stationary (fixation). 4. Many neurons in the prepositus nucleus and the medial vestibular nucleus (n = 15) were similar to abducens neurons, in that their firing rate was related primarily to horizontal eye position and eye velocity, regardless of the behavioral paradigm used. These cells were, on average, more sensitive to eye position and smooth pursuit eye velocity than were abducens neurons. 5. The firing rate of 15 other neurons in the prepositus and medial vestibular nucleus was related primarily to horizontal smooth pursuit eye movements. The tonic firing rate of all of these smooth pursuit (SP) cells was related to horizontal eye position, and the majority generated bursts of spikes during saccades in all directions but their off direction. Six of the SP neurons fired in phase with ipsilateral eye movements, whereas the remaining nine were sensitive to eye movements in the opposite direction.(ABSTRACT TRUNCATED AT 400 WORDS)

The discharge of neurons in the vestibular nuclei was recorded in alert squirrel monkeys while they were being sinusoidally rotated at 2 Hz. Type I position-vestibular-pause (PVP I) and vestibular-only (V I) neurons, as well as a smaller number of other type I and type II eye-plus-vestibular neurons were studied. Many of the neurons were monosynaptically related to the ipsilateral vestibular nerve. Eye-position and vestibular components of the rotation response were separated by multiple regression. Anodal currents, simultaneously delivered to both ears, were used to eliminate the head-rotation signals of irregularly discharging (I) vestibular-nerve afferents, presumably without affecting the corresponding signals of regularly discharging (R) afferents. R and I inputs to individual central neurons were determined by comparing rotation responses with and without the anodal currents. The bilateral currents, while reducing the background discharge of all types of neurons, did not affect the mean vestibular gain or phase calculated from a population of PVP I neurons or from a mixed population consisting of all type I units. From this result, it is concluded that I inputs are canceled at the level of secondary neurons. The cancellation may explain why the ablating currents do not affect the gain and phase of the vestibulo-ocular reflex. While cancellation was nearly perfect on a population basis, it was less so in individual neurons. For some neurons, the ablating currents decreased vestibular gain, while for other neurons the vestibular gain was increased. The former neurons are interpreted as receiving a net excitatory (I-EXC) I input, the latter neurons, a net inhibitory (I-INH) input. When compared with the corresponding R inputs, the I inputs were usually small and phase advanced. Phase advances were larger for I-EXC than for I-INH inputs. The sign and magnitude of the I inputs were unrelated to other discharge properties of individual neurons, including discharge regularity and the phase of vestibular responses measured in the absence of the ablating currents. Unilateral currents were used to assess the efficacy of ipsilateral and contralateral pathways. Ipsilateral pathways were responsible for almost all of the effects seen with bilateral currents. The results suggest that the vestibular signals carried by central neurons, even by those neurons receiving a monosynaptic vestibular-nerve input, are modified by polysynaptic pathways.

The contribution of irregular vestibular afferents to viewing distance-related changes in the angular vestibulo-ocular reflex (AVOR) and combined angular and linear VOR (CVOR) was studied in squirrel monkeys trained to fixate earth-stationary targets that were near (10 cm) and distant (90-170 cm) from their eyes. Perilymphatic anodal galvanic currents were used to reversibly silence irregular vestibular afferents for periods of 4-5 s during the AVOR and CVOR evoked by 0.5- to 4-Hz sinusoidal rotations (6-20 degrees/s peak velocity) or 250-400 degrees/s2 acceleration steps. The direction and magnitude of linear translation were changed by positioning the monkeys at different distances off the axis of turntable rotation. The effects of irregular afferent galvanic ablation (GA) on viewing distance-related changes in the AVOR were studied in four animals. Viewing distance-related changes in the AVOR could not always be evoked and were frequently small in amplitude. GA reduced viewing distance-related change in the AVOR by an average of 64% when it was present. Thus vestibular irregular afferents appear to play an important and necessary role in viewing distance-related changes in the AVOR - on those occasions when the changes occur. Viewing distance-related changes in the CVOR were large and reliably evoked. GA had very little effect on the gain or phase of viewing distance-related changes in the CVOR, although the viewing distance-related CVOR responses of individual central vestibular neurons were affected. We conclude that irregular afferents probably contribute to central signal processing related to both the AVOR and the CVOR, but the signals carried by these afferents are only essential for viewing distance-related changes in AVOR.

Spatio-temporal convergence (STC) properties of 19 vestibular only neurons' responses to translational head movements were examined in an alert, behaving squirrel monkey. In addition to standard tests that included 1.2 Hz yaw/pitch/roll rotations and inter-aural/naso-occipital/dorso-ventral translations, we also observed responses to translations along multiple directions in several orthogonal planes. Neural responses were fitted first by a model that permitted STC in all planes, characterized by a non-zero minimum and a gradual shift of phase. We then evaluated statistically whether models with fewer independent dynamic parameters yielded equally satisfactory results. The responses of 13 neurons were adequately fit by simple cosine models (1-D) as well as models that allowed complex STC behavior. Of the six neurons exhibiting STC, five could be modeled with two independent phase parameters (2-D) while the remaining neuron required a model with three independent phase parameters (3-D). The maximum translation sensitivity and phase, Smax and varphimax, and minimum translation sensitivity and phase, Smin and varphimin, were estimated from the reconstructed sensitivity and phase surfaces. The tuning ratio, Smin/Smax, in STC neurons was>0.40 while in 1-D neurons it was <0.25. Furthermore, the maximum response vectors of most 1-D neurons lay within 20 degrees of either the horizontal or sagittal plane while those of STC neurons lay >20 degrees from both planes. No difference in other response properties, such as varphimax or rotational responses, was found between neurons exhibiting STC and the simple cosine tuning. Our results suggest that the STC behavior observed in otolith-related vestibular neurons probably arises from summing inputs from afferents, with diverse response dynamics, innervating different otolith macula.

Effects of viewing distance on the responses of vestibular neurons to combined angular and linear vestibular stimulation. The firing behavior of 59 horizontal canal-related secondary vestibular neurons was studied in alert squirrel monkeys during the combined angular and linear vestibuloocular reflex (CVOR). The CVOR was evoked by positioning the animal's head 20 cm in front of, or behind, the axis of rotation during whole body rotation (0.7, 1.9, and 4.0 Hz). The effect of viewing distance was studied by having the monkeys fixate small targets that were either near (10 cm) or far (1.3-1.7 m) from the eyes. Most units (50/59) were sensitive to eye movements and were monosynaptically activated after electrical stimulation of the vestibular nerve (51/56 tested). The responses of eye movement-related units were significantly affected by viewing distance. The viewing distance-related change in response gain of many eye-head-velocity and burst-position units was comparable with the change in eye movement gain. On the other hand, position-vestibular-pause units were approximately half as sensitive to changes in viewing distance as were eye movements. The sensitivity of units to the linear vestibuloocular reflex (LVOR) was estimated by subtraction of angular vestibuloocular reflex (AVOR)-related responses recorded with the head in the center of the axis of rotation from CVOR responses. During far target viewing, unit sensitivity to linear translation was small, but during near target viewing the firing rate of many units was strongly modulated. The LVOR responses and viewing distance-related LVOR responses of most units were nearly in phase with linear head velocity. The signals generated by secondary vestibular units during voluntary cancellation of the AVOR and CVOR were comparable. However, unit sensitivity to linear translation and angular rotation were not well correlated either during far or near target viewing. Unit LVOR responses were also not well correlated with their sensitivity to smooth pursuit eye movements or their sensitivity to viewing distance during the AVOR. On the other hand there was a significant correlation between static eye position sensitivity and sensitivity to viewing distance. We conclude that secondary horizontal canal-related vestibuloocular pathways are an important part of the premotor neural substrate that produces the LVOR. The otolith sensory signals that appear on these pathways have been spatially and temporally transformed to match the angular eye movement commands required to stabilize images at different distances. We suggest that this transformation may be performed by the circuits related to temporal integration of the LVOR.