Transfer function of the rhesus macaque oculomotor system for small-amplitude slow motion trajectories

Two main types of small eye movements occur during gaze fixation: microsaccades and slow ocular drifts. While microsaccade generation has been relatively well studied, ocular drift control mechanisms are unknown. Here we explored the degree to which monkey smooth eye movements, on the velocity scale of slow ocular drifts, can be generated systematically. Two male rhesus macaque monkeys tracked a spot moving sinusoidally, but slowly, along the horizontal or vertical direction. Maximum target displacement in the motion trajectory was 30 min arc (0.5°), and we varied the temporal frequency of target motion from 0.2 to 5 Hz. We obtained an oculomotor "transfer function" by measuring smooth eye velocity gain (relative to target velocity) as a function of frequency, similar to past work with large-amplitude pursuit. Monkey eye velocities as slow as those observed during slow ocular drifts were clearly target motion driven. Moreover, as with large-amplitude smooth pursuit, eye velocity gain varied with temporal frequency. However, unlike with large-amplitude pursuit, exhibiting low-pass behavior, small-amplitude motion tracking was band pass, with the best ocular movement gain occurring at ~0.8-1 Hz. When oblique directions were tested, we found that the horizontal component of pursuit gain was larger than the vertical component. Our results provide a catalog of the control abilities of the monkey oculomotor system for slow target motions, and they also support the notion that smooth fixational ocular drifts are controllable. This has implications for neural investigations of drift control and the image-motion consequences of drifts on visual coding in early visual areas. NEW & NOTEWORTHY We studied the efficacy of monkey smooth pursuit eye movements for very slow target velocities. Pursuit was impaired for sinusoidal motions of frequency less than ~0.8-1 Hz. Nonetheless, eye trajectory was still sinusoidally modulated, even at velocities lower than those observed during gaze fixation with slow ocular drifts. Our results characterize the slow control capabilities of the monkey oculomotor system and provide a basis for future understanding of the neural mechanisms for slow ocular drifts.