Volitional control of anticipatory ocular pursuit responses under stabilised image conditions in humans

Abstract

Ocular pursuit responses have been examined in humans in three experiments in which the pursuit target image has been fully or partially stabilised on the fovea by feeding a recorded eye movement signal back to drive the target motion. The objective was to establish whether subjects could volitionally control smooth eye movement to reproduce trajectories of target motion in the absence of a concurrent target motion stimulus. In experiment 1 subjects were presented with a target moving with a triangular waveform in the horizontal axis with a frequency of 0.325 Hz and velocities of +/- 10-50 degrees/s. The target was illuminated twice per cycle for pulse durations (PD) of 160-640 ms as it passed through the centre position; otherwise subjects were in darkness. Subjects initially tracked the target motion in a conventional closed-loop mode for four cycles. Prior to the next target presentation the target image was stabilised on the fovea, so that any target motion generated resulted solely from volitional eye movement. Subjects continued to make anticipatory smooth eye movements both to the left and the right with a velocity trajectory similar to that observed in the closed-loop phase. Peak velocity in the stabilised-image mode was highly correlated with that in the prior closed-loop phase, but was slightly less (84% on average). In experiment 2 subjects were presented with a continuously illuminated target that was oscillated sinusoidally at frequencies of 0.2-1.34 Hz and amplitudes of +/- 5-20 degrees. After four cycles of closed-loop stimulation the image was stabilised on the fovea at the time of peak target displacement. Subjects continued to generate an oscillatory smooth eye velocity pattern that mimicked the sinusoidal motion of the previous closed-loop phase for at least three further cycles. The peak eye velocity generated ranged from 57-95% of that in the closed-loop phase at frequencies up to 0.8 Hz but decreased significantly at 1.34 Hz. In experiment 3 subjects were presented with a stabilised display throughout and generated smooth eye movements with peak velocity up to 84 degrees/s in the complete absence of any prior external target motion stimulus, by transferring their attention alternately to left and right of the centre of the display. Eye velocity was found to be dependent on the eccentricity of the centre of attention and the frequency of alternation. When the target was partially stabilised on the retina by feeding back only a proportion (Kf = 0.6-0.9) of the eye movement signal to drive the target, subjects were still able to generate smooth movements at will, even though the display did not move as far or as fast as the eye. Peak eye velocity decreased as Kf decreased, suggesting that there was a continuous competitive interaction between the volitional drive and the visual feedback provided by the relative motion of the display with respect to the retina. These results support the evidence for two separate mechanisms of smooth eye movement control in ocular pursuit: reflex control from retinal velocity error feedback and volitional control from an internal source. Arguments are presented to indicate how smooth pursuit may be controlled by matching a voluntarily initiated estimate of the required smooth movement, normally derived from storage of past re-afferent information, against current visual feedback information. Such a mechanism allows preemptive smooth eye movements to be made that can overcome the inherent delays in the visual feedback pathway.