Davida Teller Award Lecture 2013: The importance of prediction and anticipation in the control of smooth pursuit eye movements

Abstract

The ability of smooth pursuit eye movements to anticipate the future motion of targets has been known since the pioneering work of Dodge, Travis, and Fox (1930) and Westheimer (1954). This article reviews aspects of anticipatory smooth eye movements, focusing on the roles of the different internal or external cues that initiate anticipatory pursuit.We present new results showing that the anticipatory smooth eye movements evoked by different cues differ substantially, even when the cues are equivalent in the information conveyed about the direction of future target motion. Cues that convey an easily interpretable visualization of the motion path produce faster anticipatory smooth eye movements than the other cues tested, including symbols associated arbitrarily with the path, and the same target motion tested repeatedly over a block of trials. The differences among the cues may be understood within a common predictive framework in which the cues differ in the level of subjective certainty they provide about the future path. Pursuit may be driven by a combined signal in which immediate sensory motion, and the predictions about future motion generated by sets of cues, are weighted according to their respective levels of certainty. Anticipatory smooth eye movements, an overt indicator of expectations and predictions, may not be operating in isolation, but may be part of a global process in which the brain analyzes available cues, formulates predictions, and uses them to control perceptual, motor, and cognitive processes.

LRP predicts smooth pursuit eye movement onset during the ocular tracking of self-generated movements

“…Anticipatory smooth pursuit is often observed when the object's motion is expected. In this case, the latency of pursuit onset can be shortened and the eyes can even start moving before the target (Kowler et al 2014). Anticipatory smooth pursuit can be induced by the repeated presentation of the same motion trajectory (Kowler and Steinman 1979), by a prior cue indicating the target motion direction (de Hemptinne et al 2008), by the history of recent trials (Collins and Barnes 2009), or when the target motion is generated by the observers themselves (Steinbach 1969).…”

Weighted integration of short-term memory and sensory signals in the oculomotor system

“…By integrating visual inputs with past experience and cues, the oculomotor system can overcome sensory delays and noise to produce eye movements matching current target movement. In the pursuit system, this allows, for example, anticipatory smooth eye movements (Dodge, Travis, & Fox, 1930;Hayhoe, McKinney, Chajka, & Pelz, 2012;Kowler, Aitkin, Ross, Santos, & Zhao, 2014;Westheimer, 1954) or zero-lag smooth pursuit tracking of a sinusoidal target motion (Dodge et al, 1930;Orban de Xivry et al, 2013). In the saccadic system, predictive saccades can be observed when tracking a target jumping at a fixed frequency (Shelhamer & Joiner, 2003), or a bouncing ball (Diaz, Cooper, Rothkopf, & Hayhoe, 2013).…”

The Role of Dopamine in Anticipatory Pursuit Eye Movements: Insights from Genetic Polymorphisms in Healthy Adults

“…Control of smooth pursuit eye movements is based on a dynamic interplay between low-level retinal and high-level extraretinal signals (Barnes, 2008; Lisberger, 2010; Kowler et al, 2014). Sensory and cognitive contributions are closely interwoven, but rely on differential neuronal resources.…”

“…Some findings point to functional associations with antisaccade performance (Ettinger et al, 2008; Haraldsson et al, 2010; Kasparbauer et al, 2015), but differences foremost showed up in BOLD responses. Smooth pursuit seems ideal for studying different mechanisms involved in oculomotor control, because it relies on a sophisticated interplay between motion perception, sensorimotor transformation, and anticipatory abilities (Lisberger, 2010; Kowler et al, 2014). However, the link between both polymorphisms and individual variations in pursuit has not been investigated appropriately yet.…”

“…We acknowledge the complexity of regulatory processes during pursuit by considering selective oculomotor measures that emphasize either the role of low-level or high-level signals involved. This distinction alludes to the specific functional contributions of retinal sensory signals and extraretinal signals, including, e.g., attention, learning, prediction, or anticipation (Yasui and Young, 1975; Robinson et al, 1986; compare also Kowler et al, 2014). Low-level signals drive bottom-up control, whereas high-level signals account for top-down control.…”