Dependence of the roll angular vestibuloocular reflex (aVOR) on gravity

Abstract

Little is known about the dependence of the roll angular vestibuloocular reflex (aVOR) on gravity or its gravity-dependent adaptive properties. To study gravity-dependent characteristics of the roll aVOR, monkeys were oscillated about a naso-occipital axis in darkness while upright or tilted. Roll aVOR gains were largest in the upright position and decreased by 7-15% as animals were tilted from the upright. Thus the unadapted roll aVOR gain has substantial gravitational dependence. Roll gains were also decreased or increased by 0.25 Hz, in- or out-of-phase rotation of the head and the visual surround while animals were prone, supine, upright, or in side-down positions. Gain changes, determined as a function of head tilt, were fit with a sinusoid; the amplitudes represented the amount of the gravity-dependent gain change, and the bias, the gravity-independent gain change. Gravity-dependent gain changes were absent or substantially smaller in roll (approximately 5%) than in yaw (25%) or pitch (17%), whereas gravity-independent gain changes were similar for roll, pitch, and yaw (approximately 20%). Thus the high-frequency roll aVOR gain has an inherent dependence on head orientation re gravity in the unadapted state, which is different from the yaw/pitch aVORs. This inherent gravitational dependence may explain why the adaptive circuits are not active when the head is tilted re gravity during roll aVOR adaptation. These behavioral differences support the idea that there is a fundamental difference in the central organization of canal-otolith convergence of the roll and yaw/pitch aVORs.

Figures

Fig. 1.

A: roll eye velocities evoked by sinusoidal oscillation of animal M0091 about naso-occipital axis while upright or tilted forward and backward before (blue traces) and after (red traces) torsional angular vestibuloocular reflex (aVOR) gain was decreased in the prone position. Slow phase eye velocities are shown by solid lines while velocities during saccades are shown as thin dashed lines. Insets: head orientation relative to gravity in which corresponding traces were obtained. Numbers on the right represent the angle between the axis of oscillation and spatial horizontal where positive values – tilt forward. Positive eye velocities represent clockwise rotation relative to the subject. B and C: torsional aVOR gains (B) and gain changes (C) plotted as a function of head tilt. Note: no gravity-dependent gain changes were produced in this experiment.

Fig. 2.

A–D: torsional aVOR gains obtained before (○) and after (●) decrease in supine (nose up) position in animal M0102. E–H: gain changes expressed in percent and plotted as a function of the head orientation in four tested planes. Gain changes were fitted with a cosine function (see text for details). Changes in bias were significant in every instance (E–H), indicating changes in the gravity-independent component. Changes in the gravity-dependent component were not significant. Insets: head orientation to the axis of tilt utilized for 4 planes of head tilt.

Fig. 3.

Change in gains of the torsional (A, D, G, and J), pitch (B, E, H, and K), and yaw (C, F, I, and L) aVOR of the four animals tested in different head orientations in left-right side down (LSD-RSD, A–C) and forward-backward (D–F), and in the left anterior-right posterior canal (LA-RP, G–I), and right anterior-left posterior canal planes (RA-LP, J–L). Individual values for each of the animals in each position are shown by the gray symbols, and the sinusoidal fits to the average values across all animals are shown by the heavy black line.

Fig. 4.

A and B: gains of roll component of the eye counter-rotation evoked by in-phase (suppression, ■) or out-of-phase (enhancement, □) rotation of the monkey and the visual surround, tested at different frequencies (A) and different peak velocities (B). C and D: gains of the yaw (●, ○), and pitch (▲, ▵) eye counter-rotation evoked by in-phase (suppression, ●, ▲) or out-of-phase (enhancement, ○, □) rotation of the monkey and the visual surround tested at different frequencies (C) and peak velocities (D).

Fig. 5.

Decrease (A, C, and E) and increase (B, D, and F) of the torsional aVOR gain in side-down (A and B), supine (C and D), and prone (E and F) head orientations. Filled symbols represent data averaged for three animals. Data were fitted with a cosine (Eq. 1, black solid line) and compared with the fits made through the average changes obtained after yaw (gray solid line) and pitch (gray dashed line) aVOR adaptation in the same animals.

Fig. 6.

Three-dimensional surface of torsional aVOR gain changes obtained after the gain was decreased (A, C, and E) or increased (B, D, and F) in RSD (A and B), supine (C and D), and prone (E and F) head orientations. Maximal values are coded as a gradient of the red color, while minimal values are coded as a gradient of blue color.