Signals in vestibular nucleus mediating vertical eye movements in the monkey

Abstract

The action potentials of single neurons were recorded extracellularly throughout the rostral vestibular nuclei and subadjacent reticular formation in three alert, juvenile, rhesus monkeys. Neuronal responses were tested during a) sinusoidal pitch oscillations in darkness, b) cancellation of the vestibuloocular reflex (VOR) during similar oscillations by fixation of a target moving with the head, c) sinusoidal vertical smooth pursuit, d) vertical saccades, and e) fixation with the head stationary. Eye movements were measured using the magnetic field-search coil technique. Of the 527 neurons isolated, 318 responded to pitch oscillation and/or vertical eye movements. The latter cells could be classified into six categories. Of this group, 273 cells were recorded from for sufficient time to allow them to be fully tested and form the basis of this report. Cells were classified as follows: pure-vestibular cells with firing rates modulated only by head velocity (15%), vestibular-pause cells that were similar to the pure-vestibular cells but paused for saccades in all directions (10%), gaze-velocity cells that modulated their rates in proportion to vertical eye velocity in space (7%), position cells with rates modulated by changes in eye position in the head but that did not burst or pause during saccades (33%), position-burst cells that also carried an eye-position signal but did burst during saccades in one direction and paused in the opposite direction (15%), and position-vestibular-pause cells that carried signals proportional to eye position in the head and head velocity and paused during all saccades (20%). Most cells that carried an eye-position signal also carried an eye-velocity signal during pursuit. Position and position-burst cells could be divided into two subcategories. Position cells that also reported head velocity represented 20% of the total sample, while those without head-velocity signals made up the remaining 13%. Position-burst cells were divided into two subcategories based on their behavior during pitch oscillation in darkness. Both carried eye-velocity signals during pursuit, but only one type (8% of the total sample) also carried an eye-velocity signal during vestibular eye movements in the dark, while the other (7%) did not. Some cells in all six categories except the pure-vestibular cells responded antidromically to stimulation of the medial longitudinal fasciculus (MLF). Only the position-vestibular-pause, position-burst, and gaze-velocity cells, however, were judged to be commonly antidromically activated, suggesting that these three cell types are the major contributors to the MLF from the rostral vestibular nuclei.(ABSTRACT TRUNCATED AT 400 WORDS)

The thalamocortical vestibular system in animals and humans

“…to rotations or translations of the animals in darkness, without concurrent somatosensory signals (Marlinski and McCrea, 2008a). Similar "vestibular-only" neurons have repeatedly been described in the vestibular nuclei (Cullen et al, 2003;Tomlinson and Robinson, 1984). The existence of such neurons in thalamic nuclei suggests the presence of first-order thalamic relays containing neurons in which signals are not mixed with visual and somatosensory signals.…”

Neural Correlates of the Dependence of Compensatory Eye Movements During Translation on Target Distance and Eccentricity

“…Based on neuronal firing patterns during static fixations, 0.5-Hz smooth pursuit, and 0.5-Hz RVOR cancellation tasks (i.e., during rotation while fixating a head-fixed target that moves with the animal), VN/PH neurons were first classified into one of the following four groups (Table 1) 1984; Cullen and McCrea 1993;Fuchs and Kimm 1975;Keller and Daniels 1975;Keller and Kamath 1975;King et al 1976;McFarland and Fuchs 1992;Miles 1974;Scudder and Fuchs 1992;Tomlinson and Robinson 1984): 1) neurons (VO) that responded during vestibular stimulation without any sensitivity for eye position and smooth eye velocity; 2) neurons (PVP) that changed their firing rates during rotation and pursuit in a complementary fashion, such that they exhibited maximal firing rate modulation during stable gaze RVOR [PVP cells modulated either in phase with ipsilateral head velocity during yaw RVOR cancellation and contralaterally directed eye velocity during horizontal smooth pursuit (type I PVP) or in phase with contralateral head velocity during RVOR suppression and ipsilaterally directed eye velocity during smooth pursuit (type II PVP)]; 3) neurons (EH) that exhibited RVOR cancellation and pursuit responses in the same directions, such that the two signals cancelled or opposed each other during stable gaze RVOR [this group included cells with ipsilaterally directed eye and head velocity sensitivities (i-EH) as well as cells with contralaterally directed eye and head velocity sensitivities (c-EH)]; and 4) neurons (BT) that exhibited both static eye position and pursuit sensitivities, but did not modulate during RVOR cancellation.…”

Differential Sensorimotor Processing of Vestibulo-Ocular Signals during Rotation and Translation

“…On the basis of neural firing rates during visual fixation, smooth pursuit, and yaw or pitch rotations while an animal fixated a head-fixed target, neurons were classified into three groups (see Materials and Methods for a more detailed description). These included PV/PVP, BT, and E-H cells (Keller and Kamath, 1975;Tomlinson and Robinson, 1984;Scudder and Fuchs, 1992;Cullen and McCrea, 1993;Lisberger et al, 1994). Typical example responses from each group of eye-contra cells (i.e., type I PV/PVP, BT, and Ec-Hc neurons) have been illustrated (see Figs.…”