Human gaze stabilization during natural activities: translation, rotation, magnification, and target distance effects

Stability of images on the retina was determined in 14 normal humans in response to rotational and translational perturbations during self-generated pitch and yaw, standing, walking, and running on a treadmill. The effects on image stability of target distance, vision, and spectacle magnification were examined. During locomotion the horizontal and vertical velocity of images on the retina was <4 degrees /s for a visible target located beyond 4 m. Image velocity significantly increased to >4 degrees /s during self-generated motion. For all conditions of standing and locomotion, angular vestibulo-ocular reflex (AVOR) gain was less than unity and varied significantly by activity, by target distance, and among subjects. There was no significant correlation(P > 0.05) between AVOR gain and image stability during standing and walking despite significant variation among subjects. This lack of correlation is likely due to translation of the orbit. The degree of orbital translation and rotation varied significantly with activity and viewing condition in a manner suggesting an active role in gaze stabilization. Orbital translation was consistently antiphase with rotation at predominant frequencies <4 Hz. When orbital translation was neglected in computing gaze, computed image velocities increased. The compensatory effect of orbital translation allows gaze stabilization despite subunity AVOR gain during natural activities. Orbital translation decreased during close target viewing, whereas orbital rotation decreased while wearing telescopic spectacles. As the earth fixed target was moved closer, image velocity on the retina significantly increased (P < 0.05) for all activities except standing. Latency of the AVOR increased slightly with decreasing target distance but remained <10 ms for even the closest target. This latency was similar in darkness or light, indicating that the visual pursuit tracking is probably not important in gaze stabilization. Trials with a distant target were repeated while subjects wore telescopic spectacles that magnified vision by 1.9 or 4 times. Gain of the AVOR was enhanced by magnified vision during all activities, but always to a value less than spectacle magnification. Gain enhancement was greatest during self-generated sinusoidal motion at 0.8 Hz and was less during standing, walking, and running. Image slip velocity on the retina increased with increasing magnification. During natural activities, slip velocity with telescopes increased most during running and least during standing. Latency of the visually enhanced AVOR significantly increased with magnification (P < 0.05), probably reflecting a contribution of the visual pursuit system. The oculomotor estimate of target distance was inferred by measuring binocular convergence, as well as from monocular parallax during head translation. In darkness, target distance estimates obtained by both techniques were less accurate than in light, consistently overestimating for near and underestimating for far targets.