Tuning of gravity-dependent and gravity-independent vertical angular VOR gain changes by frequency of adaptation

Abstract

The gain of the vertical angular vestibulo-ocular reflex (aVOR) was adaptively increased and decreased in a side-down head orientation for 4 h in two cynomolgus monkeys. Adaptation was performed at 0.25, 1, 2, or 4 Hz. The gravity-dependent and -independent gain changes were determined over a range of head orientations from left-side-down to right-side-down at frequencies from 0.25 to 10 Hz, before and after adaptation. Gain changes vs. frequency data were fit with a Gaussian to determine the frequency at which the peak gain change occurred, as well as the tuning width. The frequency at which the peak gravity-dependent gain change occurred was approximately equal to the frequency of adaptation, and the width increased monotonically with increases in the frequency of adaptation. The gravity-independent component was tuned to the adaptive frequency of 0.25 Hz but was uniformly distributed over all frequencies when the adaptation frequency was 1-4 Hz. The amplitude of the gravity-independent gain changes was larger after the aVOR gain decrease than after the gain increase across all tested frequencies. For the aVOR gain decrease, the phase lagged about 4° for frequencies below the adaptation frequency and led for frequencies above the adaptation frequency. For gain increases, the phase relationship as a function of frequency was inverted. This study demonstrates that the previously described dependence of aVOR gain adaptation on frequency is a property of the gravity-dependent component of the aVOR only. The gravity-independent component of the aVOR had a substantial tuning curve only at an adaptation frequency of 0.25 Hz.

Fig. 1.

Testing of the vertical angular vestibulo-ocular reflex (aVOR) gain in various head orientations from left- (LSD) to right-side down (RSD) at 0.25 (A and D), 1 (B and E), and 10 Hz (C and F) obtained in a single experiment from animal M1. A–C: open circles represent the vertical gain before adaptation, and filled circles represent the vertical gain after it was adaptively decreased at 1 Hz in RSD position. D–F: gain changes plotted as a function of head orientation were fit with bias and sinusoid to obtain gravity-dependent and -independent gain changes. Insets below are approximate head orientations during testing. G: gravity-dependent (filled squares) and -independent gain changes (open squares) as a function of testing frequency. Solid curve is a Gaussian fit through the data. Dashed line represents the average value for the bias.

Fig. 2.

Gravity-dependent (filled squares) and -independent gain changes (open squares) plotted as a function of testing frequencies after the aVOR gain was increased (A–C) and decreased (D–F) at 0.25 (A and D), 2 (B and E), and 4 Hz (C and F). Data in A–F were obtained on different experimental days from 1 animal (M1). See text for details.

Fig. 3.

Gravity-dependent (filled squares) and -independent gain changes (open squares) plotted as a function of testing frequencies after the aVOR gain was increased (A-C) and decreased (D–F) at 0.25 (A and D), 2 (B and E), and 4 Hz (C and F). Data in A–F were obtained on different experimental days from 1 animal (M2). See text for details.

Fig. 4.

Phase changes observed after the aVOR gain decreases (A–C) and increases (D–F) induced at 0.25 (A and D), 2 (B and E), and 4 Hz (C and F). Dashed vertical gray line and arrow indicate the frequency at which the aVOR gain was adapted. Black symbols represent significant changes in phase (P < 0.05).