Y. Howard Li¹, Jonathan D. Victor², Michele Rucci¹; ¹University of Rochester, ²Weill Cornell Medical College

It is commonly assumed that the visual system encodes spatial information by the relative locations of neuronal receptive fields, beginning in the retina. The eyes, however, are never stationary; even when attending to a single point, incessant small movements (fixational drifts) also occur between saccades. A growing body of evidence indicates that spatial information is also extracted from the luminance modulations caused by eye movements. Furthermore, recent evidence suggests that the visual system can infer spatial relations from precise extraretinal knowledge of how the eye moves during fixation. How are these different sources of spatial information integrated? To investigate this question, here we decoupled eye movements from their normal luminance modulations via high-resolution eye-tracking and gaze-contingent display control. In a 2AFC orientation discrimination task, subjects were asked to report the orientation of a static grating (±45o) while maintaining fixation. Stimuli were presented with a directional inconsistency between fixational drifts and the expected temporal modulations. This was accomplished by moving the stimulus on the display according to eye movements, so that, on the retina, the stimulus moved at every moment as if the eye had drifted in a different (rotated) direction, but with the same velocity. All subjects’ performance was greatly impaired when the retinal motion and the eye trajectory differed by 90o, a manipulation that drastically alters the relationship between grating orientation and the spatiotemporal structure of the luminance fluctuations resulting from eye movements. In contrast, performance recovered approximately to normal when retinal and drift trajectories were rotated by 180o, a condition that restores consistency between luminance fluctuations resulting from eye movements and grating orientation. These results suggest that knowledge of drift direction provides critical spatial information, and a violation of the contingency between the expected and the actual retinal luminance flows is detrimental to visual processing.

Acknowledgements: This work was supported by National Institutes of Health grants EY018363, EY07977 and P30 EY001319.