How the unstable eye sees a stable and moving world: Redux

Despite incessant retinal image motion, humans reliably perceive stable and moving objects in the world. In 2013, Arathorn et al. found that the direction of stimulus motion with respect to fixational eye motion impacts the amount of motion perceived: Subjects perceived motion when stimuli moved in the same direction as eye movements and perceived little to no motion when images moved directly opposite the direction of eye motion, surprisingly even under conditions where that motion was amplified. This suggests that the visual system computes its direction of motion and perceptually renders anything moving in a direction opposite to that eye motion as stable. We asked: How is the direction of eye motion determined? Is world-fixed retinal image background content needed to compute the direction of motion or are non-visual cues (eg. efferent copy) sufficient? We explored this question using an adaptive optics scanning laser ophthalmoscope which performs high resolution eye tracking and delivers retina-contingent stimuli. We quantified perceived motion using a method of adjustment where the subject compared a stimulus moving contingent to the retina and a stimulus moving on a random walk. The subject adjusted the diffusion constant of the random walk stimulus until the perceived motion of both stimuli looked equal. Experiments were done with retinal image background content and with all visual content removed. In the presence of retinal image background content, the perceived motion of stimuli moving with a 2.5X exaggerated retinal slip was suppressed; however, in conditions with no visual content we found that a higher magnitude of motion was perceived. Our results suggest that the presence of retinal image background content provides the primary signal for the visual system to compute its direction of motion, contradicting the intuition that the same content would provide a frame of reference to see that motion.