Dynamics of binocular fixation of targets during fore-aft motion

When subjects move in the fore-aft direction, version and vergence are generated through the linear vestibulo-ocular reflex (lVOR) and pursuit systems to maintain binocular fixation. While the dynamics of pursuit and the lVOR have been studied for monocular gaze, the frequencies over which these systems operate to maintain binocular fixation are not known. The frequency characteristics of pursuit and the lVOR and their interaction were determined in two monkeys that were trained to fixate targets at vertical, lateral, and oblique positions on a computer screen. Animals were oscillated at 0.05 Hz to 4 Hz along their naso-occipital axes while fixating the targets (lVOR+pursuit). Animals were also stationary and fixated targets on the screen moving horizontally, vertically, or obliquely over ≈3° at various frequencies up to 1 Hz (pursuit). Eye movements were recorded with dual scleral search coils, and Fick angles were computed for each eye and compared to target positions. When animals pursued targets moving on the screen at low frequencies (0.05 Hz-0.5 Hz), the gains were close to unity, and the eyes were in-phase with the target. Pursuit gains decreased to ≈0.5 and phases lagged by ≈35° as the frequencies of target oscillation increased above ≈0.5 Hz. When fixating the targets during fore-aft oscillation (lVOR+pursuit), the gain was close to 1.0, and phases were within 10°-15° for frequencies up to 3 Hz. Thus, although pursuit alone does not contribute to visual following at higher frequencies, the interaction of binocular pursuit and the lVOR supported accurate binocular fixation for frequencies up to 3 Hz.