Cordelia D. Aitkin

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

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.

Anticipatory Smooth Eye Movements in Autism Spectrum Disorder

Smooth pursuit eye movements are important for vision because they maintain the line of sight on targets that move smoothly within the visual field. Smooth pursuit is driven by neural representations of motion, including a surprisingly strong influence of high-level signals representing expected motion. We studied anticipatory smooth eye movements (defined as smooth eye movements in the direction of expected future motion) produced by salient visual cues in a group of high-functioning observers with Autism Spectrum Disorder (ASD), a condition that has been associated with difficulties in either generating predictions, or translating predictions into effective motor commands. Eye movements were recorded while participants pursued the motion of a disc that moved within an outline drawing of an inverted Y-shaped tube. The cue to the motion path was a visual barrier that blocked the untraveled branch (right or left) of the tube. ASD participants showed strong anticipatory smooth eye movements whose velocity was the same as that of a group of neurotypical participants. Anticipatory smooth eye movements appeared on the very first cued trial, indicating that trial-by-trial learning was not responsible for the responses. These results are significant because they show that anticipatory capacities are intact in high-functioning ASD in cases where the cue to the motion path is highly salient and unambiguous. Once the ability to generate anticipatory pursuit is demonstrated, the study of the anticipatory responses with a variety of types of cues provides a window into the perceptual or cognitive processes that underlie the interpretation of events in natural environments or social situations.

Anticipatory smooth eye movements evoked by motor intentions

Anticipatory smooth eye movements (ASEM) are predictive smooth eye movements in the expected direction of future target motion. ASEM are evoked by various cues that signal the direction of future target motion, including cues from our own motor intentions when we move targets ourselves (Kowler et al., 2014; Ross & Santos, 2014). How do motor intentions trigger ASEM? Does the pursuit system monitor motor commands directly, or, alternatively, use motor intentions, along with other cues, to represent the expected path of future target motion? These alternatives can be distinguished by imposing visuo-motor conflicts. Subjects pursued a target disk whose motion was controlled by a mouse. The disk was moved through an inverted Y-shaped tube, with subjects choosing either the right or left oblique pathway. In the absence of visuo-motor conflict, ASEM were found before the target entered the oblique pathway. Results were similar regardless of whether the mouse steered the target, or control was limited to choosing the right or left pathway via a brief deflection of the mouse at trial onset. In the presence of visuo-motor conflict, when the target moved opposite to the hand movement, ASEM on average corresponded to the expected direction of target motion, not the direction of hand movement. Managing the visuo-motor conflict introduced costs in that ASEM were slower when the target was guided through the entire path than when control was limited to simply choosing the right or left path at trial onset. The results show that high-level expectations dominate the influence of lower-level motor commands in generating ASEM with self-moved targets. Even expectations created by a simple choice of the path are effective. The results add to the evidence that neural signals representing the strength of beliefs about the trajectory of future motion are instrumental in controlling pursuit eye movements. Meeting abstract presented at VSS 2015.