Flexibility of vestibulo-ocular reflex adaptation to modified visual input in human

Abstract

The vestibulo-ocular reflex (VOR) serves to keep images relatively stable on the retina. To maintain appropriate performance and minimize image slip throughout life, VOR is subjected to long-term adaptive regulation by visual input. It has been reported that adaptive changes in VOR gain (eye velocity/head velocity) are evoked either by fitting subjects with magnifying, miniaturizing, or reversing spectacles during normal behavior, or by moving a large visual field in or out of phase relative to the subject's head movement. The changes in VOR gain are frequency selective. Here, we examine the extent of VOR gain flexibility by causing VORs of similar direction to undergo different behavioral gain changes. Nine healthy adults participated in the study, ranging in age from 24 to 38 years (mean: 26 years) and with no history of neurotological symptoms. All subjects were clinically normal according to a screening battery that included combined neurologic and otologic physical examinations. Horizontal and vertical eye positions were recorded by bitemporal DC-coupled electro-oculography (EOG). The subject sat in a rotating chair. The axis of rotation of the body was always earth-vertical, with the interaural axis crossing the axis of rotation of the chair. The head was pointed 20° downwards in all experiments and stabilized in this position using a chin rest. The chair was surrounded by a half-cylindrical optokinetic screen (78 cm in diameter) placed in front of the subject, onto which random dot patterns were projected. Goggles were used to ensure that the subject was in complete darkness during both pre- and postadaptation periods. The chair was rotated sinusoidally at maximum amplitude of 30° or 60°: for 30° the stimulation was at 0.1, 0.2, 0.3, and 0.4 Hz; for 60° it was at 0.1, 0.2, and 0.3 Hz. VOR adaptation was obtained by inducing a retinal slip velocity by short-term alteration of the visual input of the large field; this change was produced by a combination of sinusoidal head rotation and the random dot patterns. In each adaptation session, the sinusoidal head rotation was either at 0.1 or 0.3 Hz and the amplitude was 30°. The random dot pattern was synchronized with sinusoidal head rotation in the same direction (x0 experiment) to make the retinal slip zero, and in the opposite direction to make the retinal slip twofold (x2 experiment). Therefore, a total of four adaptation protocols were tested. The subjects were asked to fixate on a single dot with the eyes straight-ahead in the x0 experiment, and follow it within random dot patterns in the x2 experiment. Each adaptation session lasted for 30 min. Two adaptation experiments were performed on each subject once per day. The averages of VOR gain and phase lag were calculated using Fourier analysis. Seven of the subjects who participated in the x2 adaptation experiment at 0.3 Hz and 30° amplitude showed a steady increase of VOR gain within a couple of trials. One of the remaining two subjects showed a decrease in VOR gain in all the three trials, and the other subject showed a VOR gain increase in three trials and decrease in two trials. In the x2 adaptation experiment at 0.3 Hz and 30° amplitude (peak velocity: 28°/s), the percentage gain change ((post−pre)/pre) was 133% at the same stimulation and 100% at 0.4 Hz (peak velocity: 37°/s). The gain change was 65% at 0.1 Hz and 60° amplitude (peak velocity: 18°/s), and 64% at 0.2 Hz and 60° amplitude (peak velocity: 37°/s). In the x1 adaptation experiment (30° at 0.3 Hz), the percentage gain change was −62% under the same conditions, −50% at 0.1 Hz and 60° amplitude, and −30% at 0.2 Hz and 60° amplitude. No change of VOR gain was observed at other frequencies, and the subject was not adapted at 0.1 Hz and 30° amplitude. The larger VOR gain increase in the x2 adaptation experiment for the faster head angular acceleration leads to the conclusion that the VOR gain mechanism can set very different gain states for the VOR that are quite similar in terms of the head acceleration.