The double-drift illusion biases the marmoset oculomotor system

Abstract

The double-drift illusion has two unique characteristics: The error between the perceived and physical position of the stimulus grows over time, and saccades to the moving target land much closer to the physical than the perceived location. These results suggest that the perceptual and saccade targeting systems integrate visual information over different time scales. Functional imaging studies in humans have revealed several potential cortical areas of interest, including the prefrontal cortex. However, we currently lack an animal model to study the neural mechanisms of location perception that underlie the double-drift illusion. To fill this gap, we trained two marmoset monkeys to fixate and then saccade to the double-drift stimulus. In line with human observers for radial double-drift trajectories with fast internal motion, we find that saccade endpoints show a significant bias that is, nevertheless, smaller than the bias seen in human perceptual reports. This bias is modulated by changes in the external and internal speeds of the stimulus. These results demonstrate that the saccade targeting system of the marmoset monkey is influenced by the double-drift illusion.

Figure 1.

Illustration of the double-drift illusion. Fast internal drift combined with slower external drift in an orthogonal direction produces a profound positional offset when viewed in the periphery. In the case where the aperture is drifting to the lower right with an internal motion that is up and right, the stimulus will appear to be moving nearly horizontally.

Figure 2.

Illustration of the DDST. (A) Marmosets were required to maintain fixation in the presence of the double-drift stimulus and then saccade to the stimulus. The stimulus was extinguished at the onset of the saccade. The top and bottom panels in the Wait period indicate the conditions with and without external motion. In the Fixation, Wait, and Saccade panels, the red circle indicates eye position. The Saccade panels illustrate that the stimulus remains on (left) up to 500 ms until a saccade is made (right). In the rightmost Saccade panel, the red line indicates eye trajectory and the red circle indicates postsaccadic eye position. (B) Diagram of the relative positions of the fixation point, stimulus path, and the fixation (2.25 dva radius) and saccade (3.5 dva radius) windows. The gray arrow indicates the stimulus path. The blue dot indicates the start position of the stimulus (nonzero external speed). The green dot indicates the position of the stimulus when the external speed is zero. (C) Illustration of saccade angle calculation. The saccade bias angle is the angle between the physical path and the saccade endpoint. Positive angles are in the direction of internal motion. (D, E) Example saccades from a marmoset to double-drift stimuli with very slow internal motion (D) and fast internal motion (E). Blue dots and red dots indicate the start and end of the saccades. The solid black and open black circles indicate the start position of the stimulus and the position of the stimulus at the time the saccade starts. The insets show a schematic of the physical path (black line), the direction of internal motion (orange arrow), and the angle of the saccade bias. (D) In this example (control condition), the internal motion is 0.1 dva/s, and there is almost no saccade error. (E) A large saccade bias angle is observed in this example with internal motion at 8 dva/s.

Figure 3.

Saccade endpoints are parametrically biased by internal and external speed. (A) Comparison of conditions with a fixed external speed of 6 dva/s and either 4 dva/s (labeled: 4/6) or 8 dva/s (labeled: 8/6) internal speed. (B) Comparison of conditions with a fixed internal speed of 8 dva/s and either 0 dva/s (green; labeled: 8/0) or 6 dva/s (blue; labeled: 8/6) external speed. (C) Summary of median angles for all three conditions. The blue dashed line shows the change observed by increasing only the internal speed. In panels B and C, blue and green indicate external speeds of 6 and 0 dva/s, respectively.