Effects of Viewing Distance on the Responses of Horizontal Canal–Related Secondary Vestibular Neurons During Angular Head Rotation

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Abstract
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°. 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.