On the relation between anticipatory ocular torsion and anticipatory smooth pursuit

Humans and other animals move their eyes in anticipation to compensate for sensorimotor delays. Such anticipatory eye movements can be driven by the expectation of a future visual object or event. Here we investigate whether such anticipatory responses extend to ocular torsion, the eyes’ rotation about the line of sight. We recorded three-dimensional eye position in head-fixed healthy human adults who tracked a rotating dot pattern moving horizontally across a computer screen. This kind of stimulus triggers smooth pursuit with a horizontal and torsional component. In three experiments, we elicited expectation of stimulus rotation by repeatedly showing the same rotation (Experiment 1), or by using different types of higher-level symbolic cues indicating the rotation of the upcoming target (Experiments 2 and 3). Across all experiments, results reveal reliable anticipatory horizontal smooth pursuit. However, anticipatory torsion was only elicited by stimulus repetition, but not by symbolic cues. In summary, torsion can be made in anticipation of an upcoming visual event only when low-level motion signals are accumulated by repetition. Higher-level cognitive mechanisms related to a symbolic cue reliably evoke anticipatory pursuit but did not modulate torsion. These findings indicate that anticipatory torsion and anticipatory pursuit are at least partly decoupled and might be controlled separately.