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Responses of vestibular-only translation sensitive (VOTS) neurons in vestibular nuclei of two squirrel monkeys were studied at multiple frequencies to three-dimensional translations and rotations. A novel frequency-dependent spatiotemporal analysis examined in each neuron whether complex models, with unrestricted response dynamics in three-dimensional (3D) space, provided significantly better fits than restricted models following simple, cosine rule. Subsequently, the statistically selected optimal model was used to predict the maximum translation direction, expressed as a unitary vector, Vt(max), and its associated sensitivity and phase across frequencies. Simple models were sufficient to quantify the 3D translational responses of 66% of neurons. Most VOTS neurons, complex or simple, exhibited flat-gain or low-pass response dynamics. The Vt(max) of simple neurons was fixed, whereas that of complex neurons changed with frequency. The spatial distribution of Vt(max) in simple neurons, which fell within 30 degrees of either the horizontal plane or/and the sagittal plane, was closely aligned with Vt(max) of vestibular afferents. In contrast, the frequency-dependent Vt(max) of most complex neurons migrated from the dorsoventral axis at higher frequency toward the horizontal plane, especially the interaural axis, at lower frequency. When the maximum rotation direction was estimated from responses of the same VOTS neurons to 1.2 Hz yaw, pitch, and roll rotations, complex neurons were more likely to respond to rotations activating vertical canals. Responses to 0.15-0.3 Hz linear accelerations produced by inertial or gravitational forces were indistinguishable in most complex neurons but significantly different in most simple neurons. These observations suggest that simple and complex VOTS neurons constitute distinctive vestibular pathways where complex neurons, exhibiting a novel spatiotemporal filtering mechanism in processing otolith-related signals, are well suited to drive tilt-related responses, whereas simple neurons probably mediate pure translation related responses.

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.

Effects of viewing distance on the responses of horizontal canal-related secondary vestibular neurons during angular head rotation. The eye movements generated by the horizontal canal-related angular vestibuloocular reflex (AVOR) depend on the distance of the image from the head and the axis of head rotation. The effects of viewing distance on the responses of 105 horizontal canal-related central vestibular neurons were examined in two squirrel monkeys that were trained to fixate small, earth-stationary targets at different distances (10 and 150 cm) from their eyes. The majority of these cells (77/105) were identified as secondary vestibular neurons by synaptic activation following electrical stimulation of the vestibular nerve. All of the viewing distance-sensitive units were also sensitive to eye movements in the absence of head movements. Some classes of eye movement-related vestibular units were more sensitive to viewing distance than others. For example, the average increase in rotational gain (discharge rate/head velocity) of position-vestibular-pause units was 20%, whereas the gain increase of eye-head-velocity units was 44%. The concomitant change in gain of the AVOR was 11%. Near viewing responses of units phase lagged the responses they generated during far target viewing by 6-25 degrees. A similar phase lag was not observed in either the near AVOR eye movements or in the firing behavior of burst-position units in the vestibular nuclei whose firing behavior was only related to eye movements. The viewing distance-related increase in the evoked eye movements and in the rotational gain of all unit classes declined progressively as stimulus frequency increased from 0.7 to 4.0 Hz. When monkeys canceled their VOR by fixating head-stationary targets, the responses recorded during near and far target viewing were comparable. However, the viewing distance-related response changes exhibited by central units were not directly attributable to the eye movement signals they generated. Subtraction of static eye position signals reduced, but did not abolish viewing distance gain changes in most units. Smooth pursuit eye velocity sensitivity and viewing distance sensitivity were not well correlated. We conclude that the central premotor pathways that mediate the AVOR also mediate viewing distance-related changes in the reflex. Because irregular vestibular nerve afferents are necessary for viewing distance-related gain changes in the AVOR, we suggest that a central estimate of viewing distance is used to parametrically modify vestibular afferent inputs to secondary vestibuloocular reflex pathways.

The firing behavior of seven antidromically identified ascending tract of Deiters (ATD) neurons was recorded in one alert squirrel monkey trained to pursue moving targets and to fixate visual targets at different distances from the head during whole body rotation. 2. ATD cells generated signals related to contralateral horizontal smooth pursuit eye movements and to ipsilateral angular and linear head velocity. Most ATD neurons reversed the direction of their response to head rotation when the vestibulo-ocular reflex was canceled by fixation of a head stationary target. 3. ATD unit gains in respect to linear head velocity increased dramatically (> 4x) when a near, earth stationary target (10 cm from the eyes) was fixated, compared to the response recorded during fixation of a far target (130 to 170 cm from the eyes). Since the viewing distance related changes in the responses of ATD neurons closely parallel the changes in the responses of the eyes, the ATD appears to be an important premotor pathway for producing viewing distance related changes in the gain of the vestibulo-ocular reflex.

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.