Dept. of Otolaryngology - Head & Neck Surgery, Johns Hopkins School of Medicine, Baltimore, MD 21287, USA.
J Physiol. 2010 Oct 15;588(Pt 20):3855-67. doi: 10.1113/jphysiol.2010.196287. Epub 2010 Aug 19.
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.
为了在头部旋转过程中保持对远距离目标的视觉固定，角前庭眼反射（aVOR）应使眼睛以与头部相同的速度并以完全相反的方向旋转。然而，对于那些已经广泛描述了三维（3D）aVOR 的灵长类动物（人类和松鼠猴（Saimiri sciureus）），当头绕额枕轴旋转时，aVOR 对滚转的反应速度低于俯仰和偏航，导致 aVOR 幅度和方向的误差随头部旋转轴而变化。换句话说，灵长类动物将视网膜中央部分的图像保持在中央凹（视锥密度和视力最高的地方），但无法防止图像绕眼球静止视轴扭曲。我们通过与外侧眼、无中央凹的哺乳动物（Chinchilla lanigera）的 aVOR 进行比较，测试了 aVOR 方向依赖性是与灵长类动物的前眼、中央凹状态相关的适应假说。由于 Chinchilla 的眼睛没有中央凹，而且永远不会相互对齐，我们预测 Chinchilla 的 aVOR 增益会相对较低，各向同性（每个头部旋转轴的增益相等）。在 11 只正常的 Chinchilla 中，我们在黑暗中记录了立体 3D 眼动，在静态倾斜（20-100 度/秒）、20-100 度/秒 1 全身体正弦旋转（0.5-15 Hz）和 3000 度/秒 2 加速度步长期间。尽管在我们检查的范围内，Chinchilla 的 3D aVOR 增益随频率和峰值速度而变化，但我们始终发现它比灵长类动物的 aVOR 更接近各向同性。我们的结果表明，灵长类动物的各向异性 aVOR 代表了对其前眼、中央凹状态的适应。在灵长类动物中，偏航和俯仰 aVOR 必须是补偿性的，以稳定两个中央凹上的图像，而滚转 aVOR 可能是补偿不足的，因为大脑可以容忍保持在中央凹上的双眼图像的扭曲。相比之下，外侧眼的 Chinchilla 面临着不同的适应需求，因此采用了不同的 aVOR 策略。
