Eye orientation during static tilts and its relationship to spontaneous head pitch in the laboratory mouse

Abstract

Both eye position and head orientation are influenced by the macular (otolith) organs, via the tilt maculo-ocular reflex (tiltMOR) and the vestibulo-collic reflexes, respectively. The mechanisms that control head position also influence the rest position of the eye because head orientation influences eye position through the tiltMOR. Despite the increasing popularity of mice for studies of vestibular and ocular motor functions, relatively little is known in this species about tiltMOR, spontaneous orientation of the head, and their interrelationship. We used 2D video oculography to determine in C57BL/6 mice the absolute horizontal and vertical positions of the eyes over body orientations spanning 360 degrees about the pitch and roll axes. We also determined head pitch during ambulation in the same animals. Eye elevation varied approximately sinusoidally as functions of pitch or roll angle. Over the central +/-30 degrees of pitch, sensitivity and gain in the light were 31.7 degrees/g and 0.53, respectively. The corresponding values for roll were 31.5 degrees/g and 0.52. Absolute positions adopted in light and darkness differed only slightly. During ambulation, mice carried the lambda-bregma plane at a downward pitch of 29 degrees , corresponding to a horizontal eye position of 64 degrees and a vertical eye position of 22 degrees . The vertical position is near the center of the range of eye movements produced by the pitch tiltMOR. The results indicate that the tiltMOR is robust in this species and favor standardizing pitch orientation across laboratories. The robust tiltMOR also has significant methodological implications for the practice of pupil-tracking video oculography in this species.

Figure 1

Effect of pitch tilts on absolute horizontal and vertical positions of the eye. 1a,c: eye positions plotted versus tilt angle of L-B axis. 1b,d: eye positions for the central ±90° of tilt replotted versus the fraction of the gravity vector projecting into the horizontal plane (the approximate plane of the utricle). On all panels, dashed lines indicate the predicted eye positions, based on the assumption that the eye counter-rotated about an axis parallel to the gimbal pitch axis. Dotted drop lines indicate eye position at a pitch of 29°, the average pitch assumed by the animals during ambulation. Error bars are 1 SD, plotted asymmetrically for graphical clarity.

Figure 2

Effect of roll tilts on absolute horizontal and vertical positions of the eye. 2a,c: eye positions plotted versus tilt angle of interocular axis. 2b,d: eye positions for the central ±90° of tilt replotted versus the fraction of the gravity vector projecting into the horizontal plane. Dashed lines indicate the eye position predicted from the simple geometrical model. Directions of roll are reported with respect to the recorded eye.

Figure 3

Demonstration of photographic and radiographic measurement of bony landmarks. 3a: Lateral photograph used to measure angle between the plane of the pedestal and the line joining the root of the maxillary incisors and the atlanto-occipital joint (∠Ped/AOJ-I). 3b: Lateral radiograph used to measure angle between lambda-bregma axis and the AOJ-I line (∠L-B/AOJ-I).