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The Journal of Neuroscience, April 26, 2006, 26(17):4519-4525; doi:10.1523/JNEUROSCI.3739-05.2006

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Behavioral/Systems/Cognitive
Anticipatory Movement Timing Using Prediction and External Cues

Jeremy B. Badler and Stephen J. Heinen

The Smith-Kettlewell Eye Research Institute, San Francisco, California 94115

Correspondence should be addressed to Stephen J. Heinen, The Smith-Kettlewell Eye Research Institute, 2318 Fillmore Street, San Francisco, CA 94115. Email: heinen{at}ski.org

Animals often make anticipatory movements to compensate for slow reaction times. Anticipatory movements can be timed using external, sensory cues, or by an internal prediction of when an event will occur. However, it is unknown whether external or internal cues dominate the anticipatory response when both are present. Smooth pursuit eye movements are generated by a motor system heavily influenced by anticipation. We measured pursuit to determine how its timing was influenced when both a predictable event and a visual cue were present. Monkeys tracked a moving target that appeared at a constant time relative to the onset of a fixation point. At a randomized time before target onset, the fixation point disappeared, creating a temporal "gap" that cued impending target motion. We found that the gap onset cue and prediction of target onset together determined pursuit initiation time. We also investigated whether prediction could override the gap onset cue or vice versa by manipulating target onset and, hence, the duration of time that the animal had to estimate to predict it. When target motion began earlier, the pursuit system relied more on prediction to trigger a movement, whereas the cue was more often used when the target moved later. Pursuit latency in previous trials partially accounted for this behavior. The results suggest that neither internal nor external factors dominate to control the anticipatory response and that the relative contributions vary with stimulus conditions. A model in which neuronal anticipation and fixation signals interact can explain the results.

Key words: smooth pursuit; eye movements; gap; expectation; interaction; primate

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Received Sept. 3, 2005; revised March 16, 2006; accepted March 17, 2006.

Correspondence should be addressed to Stephen J. Heinen, The Smith-Kettlewell Eye Research Institute, 2318 Fillmore Street, San Francisco, CA 94115. Email: heinen{at}ski.org

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