Cognitive expectations, not habits, control anticipatory smooth oculomotor pursuit

Human smooth pursuit eye movements anticipate the future path of moving targets. Anticipatory pursuit is sometimes attributed to cognitive expectations about future motion and other times to the habitual repetition of previous pursuit responses. Expectations and habits were separated by having subjects smoothly pursue a target moving along a randomly-selected path that was either undisclosed to the subject before each trial or disclosed by means of auditory or visual cues. When the path was undisclosed, the direction of anticipatory smooth eye movements was determined by the direction of target motion in the previous trial. In the presence of cues-the critical condition for separating habits and expectations-effects of previous trials diminished and anticipatory smooth eye movements were primarily determined by the direction of motion the subject was told to expect. These results show a strong contribution of cognitive expectations which overrides persevering smooth oculomotor habits. Smooth pursuit eye movements are driven by a signal that combines the present target motion with the target motion expected to occur several hundred milliseconds into the future. The expected motion is based on a genuine cognitive prediction, not lower-level sensory or motor memories of past events.