Cognitive expectation modulates ocular torsion

Purpose: Torsional eye movements are considered reflexive responses to visual image rotation or to head roll about the visual axis. Recent studies indicate that torsion scales with visual stimulus properties such as rotational direction, speed and size, indicating a voluntary component. However, it is unclear whether these eye movements can be modulated by cognitive factors such as expectation. Method: Head-fixed healthy human adults (n=6) viewed a textured disk, translating horizontally to the right across a computer monitor and rotating about its center. This type of stimulus triggers horizontal smooth pursuit eye movements with a torsional component. Stimulus rotation was either clockwise, in the same direction as a rolling ball (“natural”), or counterclockwise (“unnatural”). In baseline trials, the texture moved horizontally without rotation. These three rotation conditions were presented in separate blocks of 100 trials each, two blocks per condition, to elicit cognitive expectation of rotational direction. Three-dimensional eye position was recorded with a head-mounted Chronos eye tracker. Results: Observers initiated horizontal pursuit 250 ms prior to stimulus onset in anticipation of translational stimulus motion. This effect was stronger for baseline than for rotation conditions, indicating that stimulus rotation is taken into account when computing anticipatory horizontal pursuit velocity. Interestingly, the eyes also started rotating clockwise in response to “natural” and counterclockwise in response to “unnatural” rotation prior to stimulus onset in anticipation of stimulus rotation.  Conclusions: Torsional eye movements can be modulated by cognitive factors, indicating a strong voluntary component in the control of these movements. The frontal pursuit pathway, including areas such as the frontal eye field, might carry ocular torsion signals and underlie the effects of cognitive expectation on ocular torsion.