Visually Induced Adaptation in Three-Dimensional Organization of Primate Vestibuloocular Reflex

Abstract

Angelaki, Dora E. and Bernhard J. M. Hess. Visually induced adaptation in three-dimensional organization of primate vestibulo-ocular reflex. J. Neurophysiol. 79: 791–807, 1998. The adaptive plasticity of the spatial organization of the vestibuloocular reflex (VOR) has been investigated in intact and canal-plugged primates using 2-h exposure to conflicting visual (optokinetic, OKN) and vestibular rotational stimuli about mutually orthogonal axes (generating torsional VOR + vertical OKN, torsional VOR + horizontal OKN, vertical VOR + horizontal OKN, and horizontal VOR + vertical OKN). Adaptation protocols with 0.5-Hz (±18°) head movements about either an earth-vertical or an earth-horizontal axis induced orthogonal response components as high as 40–70% of those required for ideal adaptation. Orthogonal response gains were highest at the adapting frequency with phase leads present at lower and phase lags present at higher frequencies. Furthermore, the time course of adaptation, as well as orthogonal response dynamics were similar and relatively independent of the particular visual/vestibular stimulus combination. Low-frequency (0.05 Hz, vestibular stimulus: ±60°; optokinetic stimulus: ±180°) adaptation protocols with head movements about an earth-vertical axis induced smaller orthogonal response components that did not exceed 20–40% of the head velocity stimulus (i.e., ∼10% of that required for ideal adaptation). At the same frequency, adaptation with head movements about an earth-horizontal axis generated large orthogonal responses that reached values as high as 100–120% of head velocity after 2 h of adaptation (i.e., ∼40% of ideal adaptation gains). The particular spatial and temporal response characteristics after low-frequency, earth-horizontal axis adaptation in both intact and canal-plugged animals strongly suggests that the orienting (and perhaps translational) but not inertial (velocity storage) components of the primate otolith-ocular system exhibit spatial adaptability. Due to the particular nested arrangement of the visual and vestibular stimuli, the optic flow pattern exhibited a significant component about the third spatial axis (i.e., orthogonal to the axes of rotation of the head and visual surround) at twice the oscillation frequency. Accordingly, the adapted VOR was characterized consistently by a third response component (orthogonal to both the axes of head and optokinetic drum rotation) at twice the oscillation frequency after earth-horizontal but not after earth-vertical axis 0.05-Hz adaptation. This suggests that the otolith-ocular (but not the semicircular canal-ocular) system can adaptively change its spatial organization at frequencies different from those of the head movement.