Coding of Velocity Storage in the Vestibular Nuclei

Sergei B Yakushin, Theodore Raphan, Bernard Cohen, Sergei B Yakushin, Theodore Raphan, Bernard Cohen

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.

Keywords: adaptation; gravity; monkey; optokinetic after-nystagmus; spatial orientation; velocity storage; vestibular-only neurons; vestibule–ocular reflex.

Figures

Figure 1
Figure 1
Three-dimensional model of velocity storage integrator. G0 represents vestibular input to the integrator (gray area), G1 represents direct vestibular, and G2 direct optokinetic pathways; H0 represents the leak of the integrator. See text for details.
Figure 2
Figure 2
(A,B) Typical examples of the resting firing rates from several neurons during the experiments. (C,D) Raster’s of firing rate of the position-vestibular-pause (PVP) neuron during spontaneous saccades to the left (C) and to the right (D). This PVP neuron paused it firing at the beginning of each saccade.
Figure 3
Figure 3
(A,B) Gains (A) and phases (B) obtained from a typical vestibular-only neuron during sinusoidal oscillation in darkness (VOR darkness, filled circles) and oscillation in light with the subject-fixed visual surround (VOR cancelation, filled triangles). (C) Activity of the same neuron recorded during sinusoidal oscillation of optokinetic surround at 0.02 Hz [optokinetic nystagmus (OKN)].
Figure 4
Figure 4
Changes in neuronal firing rate of three vestibular-only neurons located in the left (A) and right (B,C) hemispheres in response to head rotation to the right [(E), negative velocity] and to the left (positive velocity) in darkness. (D) Superimposed eye velocities for 10 repeated rotations. Gray—original eye velocities. Black—slow phase eye velocities. See details in the text. (F) Relationship between average sensitivity to rotation toward ipsilateral (abscissa) and contralateral (ordinate) sides. Black symbols—neurons with identical sensitivities to rotation in both directions (p < 0.05). Gray symbols—neurons with asymmetrical sensitivities.
Figure 5
Figure 5
Changes in the firing rate of a typical vestibular-only (VO) neuron that codes the yaw component of velocity storage during head rotation at 60°/s (A), 90°/s (B), and 120°/s (C). (A–C) In each section, after being in darkness for 5 s, the animal was rotated to the left (counterclockwise) and then stopped while in darkness (primate position, tooth-like, and constant levels, respectively). Then rotation was repeated in the opposite (clockwise) direction. This sequence induces per-rotatory nystagmus to the right (Negative Eye Velocity) which gradually declined to 0. When rotation was stopped, it induces post-rotatory nystagmus in the opposite direction (positive eye velocity). This sequence of per- and post-rotatory nystagmus was repeated in the opposite directions. The experiment animal was extremely drowsy, and there was a sudden decline of slow phase eye velocities to 0. Drowsiness, however, did not the affect firing rate of this VO neuron. (D) Relationship between the time constants of velocity storage determined from slow the phase eye velocity (ordinate) and from the neuronal firing rate (abscissa). Each data point on this graph represents a time constant measured for the oculomotor response and corresponding neuronal response. This is shown in the two responses in graphs (A–C). The black line is the linear regression of the data.
Figure 6
Figure 6
(A) Changes in the neuronal firing rate induced by head rotation about a spatial vertical axis of vestibular-only neuron that does not code the yaw component of velocity storage. See also legend to Figure 5 for details. (B) Changes in the time constant determined from yaw slow phase eye velocities (ordinate) did not correlate with changes determined from the neuronal firing rate (abscissa).
Figure 7
Figure 7
Left posterior canal-related neuron tested by sinusoidal oscillation (A–C) and by step rotation (D–F) about a spatial vertical axis while the animal was upright (A,D), tilted left side down (B,E), or tilted left side down and then rotated 90° counterclockwise in yaw to bring the right anterior–left posterior canals to the plane of rotation (C,F).
Figure 8
Figure 8
(A,B) Relationship of the time constant of velocity storage measured from the yaw slow phase eye velocity (abscissa) during vestibular nystagmus (A) and optokinetic after-nystagmus (OKAN) (B) and measured from the changes in the neuronal firing rate (ordinate). The individual lines are regression lines for the vestibular-only (black) and VPS (red) neurons. (C) Relationship between the time constant of the yaw component of velocity storage tested with 60°/s optokinetic nystagmus/OKAN while the head was tilted side down at various degrees up to 90°. The time constant of the decline in neuronal firing is shown in Figure 9.
Figure 9
Figure 9
Changes in the firing rate (Unit FR) of a Type II vestibular-only neuron that receives convergent inputs from the otolith and the contralateral, lateral, and anterior canals. The neuron was tested in the left side down (A–D) and right side down (E–H) positions. For each position, the neuron was tested while upright (A,E) or while tilted 30° (B,F), 60° (C,G), or 90° (D,H). The firing rate decrease in response to optokinetic nystagmus (OKN)/OKAN to the right [(A-D), unit FR] and increased in response to OKN/OKAN to the left [(E–H), unit FR]. In a tilted position, the duration of the yaw component of OKAN decreased with the tilt angle (V yaw), and there was a cross-coupled vertical component (V pitch). Changes in the firing rate of this neuron were only associated with changes in V yaw.
Figure 10
Figure 10
Changes in the firing rate (Unit FR) of a VPS neuron that received convergent input from the contralateral posterior canal during optokinetic nystagmus (OKN)/OKAN in the left side down (A–C) or right side down (D–F) positions. For each position, the neuron was tested while upright (A,D) or while tilted 30° (B,E) or 60° (C,F). (A,D) are replicated from the same data. V yaw is the yaw slow phase eye velocity and V pitch is the slow phase pitch eye velocity. ON denotes the OKN interval, and OFF denotes the OKAN interval. Data in panel (D) are duplicate of panel (A). This was done to organize data in columns to simplify comparison.
Figure 11
Figure 11
Unit firing rates and yaw (V yaw), pitch (V pitch), and roll (V pitch) slow phase eye velocities for a VPS neuron that received input from the ipsilateral anterior canal during optokinetic nystagmus (OKN)/optokinetic after-nystagmus to the left (A–H) and to the right (I–P). This neuron was tested in the left side down (A–D,I–L) and supine (E–H,M–P) positions. In each position, the neuron was tested while upright (A,E,I,M) or while tilted 30° (B,F,J,N), 60° (C,G,K,O), or 90° (D,H,L,P). Data in panel (E) are duplicate of panel (A), and data in panel (M) are duplicate of panel (I). This was done to organize data in columns to simplify comparison.

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Source: PubMed

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