Anticipatory Movement Timing Using Prediction and External Cues

Abstract

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.

Trial-by-Trial Updating of the Gain in Preparation for Smooth Pursuit Eye Movement Based on Past Experience in Humans

“…This is consistent with previous reports regarding anticipatory drift (Badler and Heinen 2006;Heinen et al 2005;Kowler et al 1984). However, the effect of the previous pursuit direction on the visually driven component was unclear.…”

“…In human subjects, it is well known that smooth eye movements, or so-called anticipatory drift, are elicited toward the direction of the expected target motion, even when the direction of this motion is not predictable (Kowler et al 1979a,b). Under unpredictable conditions, the magnitude of the anticipatory drift is influenced by the previous tracking direction (Badler and Heinen 2006;Heinen et al 2005;Kowler et al 1984). Such effects of past experiences on motor generation have also been reported in other motor behaviors, such as saccadic eye movements (Dorris et al 1999;Fecteau and Munoz 2003;McPeek et al 1999;Paré and Munoz 1996), canceling of eye movements (Emeric et al 2007;Kornylo et al 2003), and grip force (Witney et al 2001).…”

Neuronal Bases of Directional Expectation and Anticipatory Pursuit

“…Anticipatory smooth pursuit is a slow movement of the eyes occurring before the appearance of an expected moving target. It has been shown repeatedly that primates can generate anticipatory smooth pursuit in the absence of visual stimulation provided there is a strong expectation about the characteristics of upcoming target motion (Kowler andSteinman, 1979a,b, 1981;Kowler et al, 1984;Kowler, 1989;Barnes and Asselman, 1991;Barnes et al, 2002;Heinen et al, 2005;Badler and Heinen, 2006;de Hemptinne et al, 2007). The influence of expectation in the spatial domain is often studied by providing information using color cues that allow subjects to orient attention to the upcoming spatial position of a target (Posner, 1980).…”

How Do Primates Anticipate Uncertain Future Events?

“…Anticipatory pursuit is a smooth movement of the eye initiated in expectation of the appearance of a moving target (Kowler, 1989). Primates can generate robust anticipatory smooth-pursuit eye movements in the absence of visual stimulation if characteristics like direction, timing, and/or velocity of the upcoming moving target are made predictable (Barnes and Asselman, 1991;Blohm et al, 2003;Missal and Heinen, 2004;Heinen et al, 2005;Badler and Heinen, 2006;de Hemptinne et al, 2006).…”