Orienting eye movements of the rabbit

Orienting vestibulo-ocular reflexes (VOR) in three-dimensions were assessed in rabbits using various techniques of generating linear and angular accelerations. During otolith stimulation by static tilt and off-vertical axis rotation (OVAR), both ocular roll and pitch tended to maintain the visual streak of the retina near the spatial horizontal by aligning the eyes with gravito-inertial acceleration (GIA). Simultaneous stimulation of the otoliths and semicircular canals during dynamic rolling and pitching about a horizontal axis increased the gain of ocular-counter rotation and expanded the frequency range of response, adjusting the orientation dynamics for active motion. A new otolith stimulus, sinusoidal translation while rotating (TWR), that combines translational, centripetal and Coriolis accelerations was developed. In response to TWR, the eyes oriented toward the GIA as during static and dynamic tilts and OVAR. A comparison between tilts and centrifugation indicated that linear accelerations in all directions contribute to ocular orientation. OVAR and TWR induced continuous nystagmus with slow phases in the direction of the rotating linear acceleration vectors, which was superimposed on the orienting eye position modulations. Similarly, the nystagmus generated by stimulation of the semicircular canals with angular acceleration about the earth-vertical axis was superimposed on orienting eye position changes in pitch, yaw vergence and version. Binocular vision was modulated by ocular pitch and yaw vergence in all test paradigms and is likely to have an important use in the rabbit's normal behavior. Despite the importance of aligning the head and eye movements to stabilize vision, the eyes rotated about axes that did not compensate the head movements during orienting reflexes. Thus the significance of orienting the eyes appeared to extend beyond the need for perfect compensation. Asymmetries between the two eyes during various types of vestibular stimulation further deviated the eyes from a perfect compensation. Eye velocity asymmetries during earth-vertical axis rotation were consistent with the well-known asymmetry of the optokinetic response in the rabbit and are likely to support vision. In summary, this study demonstrates that the rabbit orients the eyes in three dimensions to support vision in response to linear and angular accelerations during various types of head motions.