Eye movements during combined pursuit, optokinetic and vestibular stimulation in macaque monkey

During natural behaviour in a visual environment, smooth pursuit eye moveme nts (SP) usually override the vestibular-ocular reflex (VOR) and the optoki netic reflex (OKR), which stem from head-in-space and scene-relative-to-eye motion, respectively. We investigated the interaction of SP, VOR, and OKR, which is not fully understood to date. Eye movements were recorded in two macaque monkeys while applying various combinations of smooth eye pursuit, vestibular and optokinetic stimuli (sinusoidal horizontal rotations of visu al target, chair and optokinetic pattern, respectively, at 0.025, 0.05, 0.1 , 0.2, 0.4, and 0.8 Hz, corresponding to peak stimulus velocities of 1.25-4 0 degrees/s for a standard stimulus of +/-8 degrees). Slow eye responses we re analysed in terms of gain and phase During CP at mid-frequencies the eye s were almost perfectly on target (,oain 0.98 at 0.1 Hz), independently of a concurrent vestibular or optokinetic stimulus. Pursuit gain at lower freq uencies, although being almost ideal (0.98 at 0.025 Hz with pursuit-only st imulation), became modified by the optokinetic input (gain increase above u nity when optokinetic stimulus had the same direction as target, decrease w ith opposite direction). At higher stimulus frequencies, pursuit,oain decre ased (down to 0.69 at 0.8 Hz), and the pursuit response became modified by vestibular input (gain increase during functionally synergistic combination s, decrease in antagonistic combinations). Thus, the pursuit system in monk ey dominates during SP-OKR-VOR in teraction, but it does so effectively onl y in the mid-fn- quency range. The results can be described in the form of a simple dynamic model in which it is assumed that the three systems intera ct by linear summation. In the model SP and OKR dominate VOR in the low- to midfrequency/velocity range, because they represent closed loop systems wi th high internal gain values (>>) at these frequencies/velocities, whereas the VOR represents an open loop system with about unity-gain (up to very hi gh frequencies). SP dominance over OKR is obtained by allowing an 'attentio nal/volitional' mechanism to boost SP gain and a predictive mechanism to im prove its dynamics.