Anticipatory smooth eye movements in autism spectrum disorder

Abstract

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.

Figure 1. Stimulus Display for Cued Target Motion.

The disc moves down the tube and then travels down whichever branch (left or right) is not blocked by the visual barrier cue.

Figure 2. Representative Eye Traces During Fixation and During Smooth Pursuit.

(Left) Representative record showing horizontal (H) and vertical (V) eye movements over time during 5 seconds of fixation of the stationary target. Participant ASD7. (Right) Representative record showing horizontal (H) and vertical (V) eye movements during 1.3 seconds of smooth pursuit of the disc moving down the tube; cued condition. The disc entered the right oblique branch at time  =  0. Participant ASD4. The vertical lines represent computer-generated markers showing beginning and end of saccades. Upward deflections indicate movements to the right or up. The separation between tic marks on the ordinate are 1 degree (60 min arc). Horizontal anticipatory smooth eye movements to the right, in the direction of cued motion, can be seen prior to time = 0 in the graph on the right.

Figure 3. Mean Eye Velocity Over Time, Motion in Cued Directions.

Mean horizontal eye velocity (average of participant means) when the visual barrier cue indicated the future path of the moving disc (left or right), for ASD (blue and green lines) and typical (red and purple lines) participants. The dotted line indicates the horizontal velocity of the disc. The disc entered the oblique branch at time  = 0 and traveled either to the right (positive values) or left (negative values) Shading indicates +/− Standard Error.

Figure 4. Mean Eye Velocity Over Time, Motion in Uncued Directions.

Mean horizontal eye velocity (average of participant means) when no cue indicated the future path of the moving disc (left or right), for ASD (blue and green lines) and typical (red and purple lines) participants. The dotted line indicates the horizontal velocity of the disc. The disc entered the oblique branch at time  = 0 and traveled either to the right (positive values) or left (negative values) Shading indicates +/− Standard Error.

Figure 5. Saccades During Maintained Fixation.

(A) Saccade vector sizes in ASD group (B) Saccade rates in ASD group. (C) Saccade sizes in Typical group. (D) Saccade rates in Typical group.