Similar Kinematic Properties for Ocular Following and Smooth Pursuit Eye Movements

Abstract

Ocular following (OFR) is a short-latency visual stabilization response to the optic flow experienced during self-motion. It has been proposed that it represents the early component of optokinetic nystagmus (OKN) and that it is functionally linked to the vestibularly driven stabilization reflex during translation (translational vestibuloocular reflex, TVOR). Because no single eye movement can eliminate slip from the whole retina during translation, the OFR and the TVOR appear to be functionally related to maintaining visual acuity on the fovea. Other foveal-specific eye movements, like smooth pursuit and saccades, exhibit an eye-position-dependent torsional component, as dictated by what is known as the "half-angle rule" of Listing's law. In contrast, eye movements that stabilize images on the whole retina, such as the rotational vestibuloocular reflex (RVOR) and steady-state OKN do not. Consistent with the foveal stabilization hypothesis, it was recently shown that the TVOR is indeed characterized by an eye-position-dependent torsion, similar to pursuit eye movements. Here we have investigated whether the OFR exhibits three-dimensional kinematic properties consistent with a foveal response (i.e., similar to the TVOR and smooth pursuit eye movements) or with a whole-field stabilization function (similar to steady-state OKN). The OFR was elicited using 100-ms ramp motion of a full-field random dot pattern that moved horizontally at 20, 62, or 83 degrees/s. To study if an eye-position-dependent torsion is generated during the OFR, we varied the initial fixation position vertically within a range of +/-20 degrees . As a control, horizontal smooth pursuit eye movements were also elicited using step-ramp target motion (10, 20, or 30 degrees/s) at similar eccentric positions. We found that the OFR followed kinematic properties similar to those seen in pursuit and the TVOR with the eye-position-dependent torsional tilt of eye velocity having slopes that averaged 0.73 +/- 0.16 for OFR and 0.57 +/- 0.12 (means +/- SD) for pursuit. These findings support the notion that the OFR, like the TVOR and pursuit, are foveal image stabilization systems.