Coding of Velocity Storage in the Vestibular Nuclei.

Sergei B Yakushin,Theodore Raphan,Bernard Cohen

doi:10.3389/fneur.2017.00386

Sergei B Yakushin, Theodore Raphan + Show 1 more

Open Access

https://doi.org/10.3389/fneur.2017.00386

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Abstract

Semicircular canal afferents sense angular acceleration and output angular velocity with a short time constant of ≈4.5 s. This output is prolonged by a central integrative network, velocity storage that lengthens the time constants of eye velocity. This mechanism utilizes canal, otolith, and visual (optokinetic) information to align the axis of eye velocity toward the spatial vertical when head orientation is off-vertical axis. Previous studies indicated that vestibular-only (VO) and vestibular-pause-saccade (VPS) neurons located in the medial and superior vestibular nucleus could code all aspects of velocity storage. A recently developed technique enabled prolonged recording while animals were rotated and received optokinetic stimulation about a spatial vertical axis while upright, side-down, prone, and supine. Firing rates of 33 VO and 8 VPS neurons were studied in alert cynomolgus monkeys. Majority VO neurons were closely correlated with the horizontal component of velocity storage in head coordinates, regardless of head orientation in space. Approximately, half of all tested neurons (46%) code horizontal component of velocity in head coordinates, while the other half (54%) changed their firing rates as the head was oriented relative to the spatial vertical, coding the horizontal component of eye velocity in spatial coordinates. Some VO neurons only coded the cross-coupled pitch or roll components that move the axis of eye rotation toward the spatial vertical. Sixty-five percent of these VO and VPS neurons were more sensitive to rotation in one direction (predominantly contralateral), providing directional orientation for the subset of VO neurons on either side of the brainstem. This indicates that the three-dimensional velocity storage integrator is composed of directional subsets of neurons that are likely to be the bases for the spatial characteristics of velocity storage. Most VPS neurons ceased firing during drowsiness, but the firing rates of VO neurons were unaffected by states of alertness and declined with the time constant of velocity storage. Thus, the VO neurons are the prime components of the mechanism of coding for velocity storage, whereas the VPS neurons are likely to provide the path from the vestibular to the oculomotor system for the VO neurons.

Highlights

When subjects are rotated, the hair cells in the semicircular canals respond to angular acceleration
Located in the medial and superior vestibular nucleus (SVN), it has an additional component, evident in primates and some mammals, namely a mechanism that orients the axis of eye rotation and probably balance to the spatial vertical
There is no reason to hypothesize that the velocity storage mechanism is involved in separating tilt from translation

Summary

Introduction

The hair cells in the semicircular canals respond to angular acceleration. The sense of rotation, the neural activity in the vestibular nuclei, and the nystagmus generated by a step in head velocity rotation has a time constant of at least 15–25 s, indicating that there is central vestibular processing that lengthens the response time [2,3,4]. The neural mechanism that converts the small time constant response at the canal afferents to the long time constant response found at the level of the vestibular nuclei, has been termed “a velocity storage integrator” [5,6,7]. Rotation in light activates velocity storage from both of these modalities so that as the vestibular drive from the semicircular canals wanes, the visual system continues to drive velocity storage generating optokinetic nystagmus (OKN) [6, 8]. When the lights are extinguished, the optokinetic after-nystagmus (OKAN) has a time constant similar to that induced in darkness by rotation at the same velocity [6, 8, 10]

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