Format

Send to

Choose Destination
J Physiol. 2010 Oct 15;588(Pt 20):3855-67. doi: 10.1113/jphysiol.2010.196287. Epub 2010 Aug 19.

Adaptation of the vestibulo-ocular reflex for forward-eyed foveate vision.

Author information

1
Dept. of Otolaryngology - Head & Neck Surgery, Johns Hopkins School of Medicine, Baltimore, MD 21287, USA.

Abstract

To maintain visual fixation on a distant target during head rotation, the angular vestibulo-ocular reflex (aVOR) should rotate the eyes at the same speed as the head and in exactly the opposite direction. However, in primates for which the 3-dimensional (3D) aVOR has been extensively characterised (humans and squirrel monkeys (Saimiri sciureus)), the aVOR response to roll head rotation about the naso-occipital axis is lower than that elicited by yaw and pitch, causing errors in aVOR magnitude and direction that vary with the axis of head rotation. In other words, primates keep the central part of the retinal image on the fovea (where photoreceptor density and visual acuity are greatest) but fail to keep that image from twisting about the eyes' resting optic axes. We tested the hypothesis that aVOR direction dependence is an adaptation related to primates' frontal-eyed, foveate status through comparison with the aVOR of a lateral-eyed, afoveate mammal (Chinchilla lanigera). As chinchillas' eyes are afoveate and never align with each other, we predicted that the chinchilla aVOR would be relatively low in gain and isotropic (equal in gain for every head rotation axis). In 11 normal chinchillas, we recorded binocular 3D eye movements in darkness during static tilts, 20-100 deg s(1) whole-body sinusoidal rotations (0.5-15 Hz), and 3000 deg s(2) acceleration steps. Although the chinchilla 3D aVOR gain changed with both frequency and peak velocity over the range we examined, we consistently found that it was more nearly isotropic than the primate aVOR. Our results suggest that primates' anisotropic aVOR represents an adaptation to their forward-eyed, foveate status. In primates, yaw and pitch aVOR must be compensatory to stabilise images on both foveae, whereas roll aVOR can be under-compensatory because the brain tolerates torsion of binocular images that remain on the foveae. In contrast, the lateral-eyed chinchilla faces different adaptive demands and thus enlists a different aVOR strategy.

PMID:
20724359
PMCID:
PMC3000578
DOI:
10.1113/jphysiol.2010.196287
[Indexed for MEDLINE]
Free PMC Article

Supplemental Content

Full text links

Icon for Wiley Icon for PubMed Central
Loading ...
Support Center