Timing and velocity randomization similarly affect anticipatory pursuit

Abstract

Smooth pursuit eye movements are guided largely by retinal-image motion. To compensate for neural conduction delays, the brain employs a predictive mechanism to generate anticipatory pursuit that precedes target motion (E. Kowler, 1990). A critical question for interpreting neural signals recorded during pursuit concerns how this mechanism is interfaced with sensorimotor processing. It has been shown that the predictor is not simply turned-off during randomization because anticipatory eye velocity remains when target velocity is randomized (E. Kowler & S. McKee, 1987; G. W. Kao & M. J. Morrow, 1994). This study was completed to compare pursuit behavior during randomized motion-onset timing with that occurring during direction or speed randomization. We found that anticipatory eye velocity persisted despite motion-onset randomization, and that anticipation onset time was between that observed in the different constant-timing conditions. This centering strategy was similar to the bias of eye velocity magnitude away from extremes observed when direction or speed was randomized. Such a strategy is comparable to least-squares error minimization, and could be used to facilitate acquisition of a target when it begins to move. Centering was in some observers accounted for by a shift of eye velocity toward that generated in the preceding trial. The results make unlikely a model in which the predictor is disengaged by randomizing stimulus timing, and suggest that predictive signals always interact with those used in sensorimotor processing during smooth pursuit.

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).…”

“…There are studies of the effects of immediate past events on the upcoming motor generation, and these effects of previous trials have been interpreted as the consequences of priming or learning, although few have addressed the question of how many preceding trials shape upcoming movement (Dorris et al 1999;Fecteau and Munoz 2003;Heinen et al 2005;Kowler et al 1984). Witney et al (2001) demonstrated that the magnitude of anticipatory grip force is affected by experiences from at least the previous three trials, but they could not directly show its on-line modulation because the fluctuation of pure anticipatory grip force could not be continuously measured.…”

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).…”

Anticipatory Movement Timing Using Prediction and External Cues

“…Nonhuman primates can also use smooth pursuit to anticipate the onset of a moving target (Missal and Heinen, 2004). Anticipation is enhanced when targets are predictable (Kowler et al, 1984;Kowler, 1989;Barnes and Asselman, 1991;Kao and Morrow, 1994;Barnes and Donelan, 1999;Heinen et al, 2005), when targets move at high speeds (Kao and Morrow, 1994;Heinen et al, 2005), and when a time delay ("gap") is present between fixation point disappearance and target appearance (Boman and Hotson, 1988). Anticipatory pursuit is also triggered by sensory cues that reliably precede target motion onset, even when the onset itself is not predictable (Kowler, 1989;Barnes and Donelan, 1999).…”