Characterization of the 3D angular vestibulo-ocular reflex in C57BL6 mice

Abstract

We characterized the three-dimensional angular vestibulo-ocular reflex (3D aVOR) of adult C57BL6 mice during static tilt testing, sinusoidal, and high-acceleration rotations and compared it with that of another lateral-eyed mammal with afoveate retinae (chinchilla) and two primate species with forward eye orientation and retinal foveae (human and squirrel monkey). Noting that visual acuity in mice is poor compared to chinchillas and even worse compared to primates, we hypothesized that the mouse 3D aVOR would be relatively low in gain (eye-velocity/head-velocity) compared to other species and would fall off for combinations of head rotation velocity and frequency for which peak-to-peak position changes fall below the minimum visual angle resolvable by mice. We also predicted that as in chinchilla, the mouse 3D aVOR would be more isotropic (eye/head velocity gain independent of head rotation axis) and better aligned with the axis of head rotation than the 3D aVOR of primates. In 12 adult C57BL6 mice, binocular 3D eye movements were measured in darkness during whole-body static tilts, 20-100°/s whole-body sinusoidal rotations (0.02-10 Hz) and acceleration steps of 3,000°/s² to a 150°/s plateau (dominant spectral content 8-12 Hz). Our results show that the mouse has a robust static tilt counter-roll response gain of ~0.35 (eye-position Δ/head-position Δ) and mid-frequency aVOR gain (~0.6-0.8), but relatively low aVOR gain for high-frequency sinusoidal head rotations and for steps of head rotation acceleration (~0.5). Due to comparatively poor static visual acuity in the mouse, a perfectly compensatory 3D aVOR would confer relatively little benefit during high-frequency, low-amplitude movements. Therefore, our data suggest that the adaptive drive for maintaining a compensatory 3D aVOR depends on the static visual acuity in different species. Like chinchillas, mice have a much more nearly isotropic 3D aVOR than do the primates for which comparable data are available. Relatively greater isotropy in lateral-eyed species without retinal foveae (e.g., mice and chinchillas in the present study) compared to forward-eyed species with retinal foveae (e.g., squirrel monkeys and humans) suggests that the parallel resting optic axes and/or radially symmetric retinal foveae of primates underlie their characteristically low 3D aVOR gain for roll head rotations.