Our eyes are constantly in motion. Even during visual fixation, small eye movements continually jitter the location of gaze1,2,3,4. It is known that visual percepts tend to fade when retinal image motion is eliminated in the laboratory5,6,7,8,9. However, it has long been debated whether, during natural viewing, fixational eye movements have functions in addition to preventing the visual scene from fading10,11,12,13,14,15,16,17. In this study, we analysed the influence in humans of fixational eye movements on the discrimination of gratings masked by noise that has a power spectrum similar to that of natural images. Using a new method of retinal image stabilization18, we selectively eliminated the motion of the retinal image that normally occurs during the intersaccadic intervals of visual fixation. Here we show that fixational eye movements improve discrimination of high spatial frequency stimuli, but not of low spatial frequency stimuli. This improvement originates from the temporal modulations introduced by fixational eye movements in the visual input to the retina, which emphasize the high spatial frequency harmonics of the stimulus. In a natural visual world dominated by low spatial frequencies, fixational eye movements appear to constitute an effective sampling strategy by which the visual system enhances the processing of spatial detail.
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We thank E. Ahissar, G. Desbordes, W. S. Geisler, K. J. Nielsen, E. L. Schwartz, D. M. Snodderly and J. D. Victor for help. This work was supported by grants from the National Institute of Health and the National Science Foundation to M.R.
Reprints and permissions information is available at www.nature.com/reprints. The authors declare no competing financial interests.
This file contains Supplementary Figures 1-2 with Legends, Supplementary Methods and Supplementary Video Legends. The two Supplementary Figures show contrast sensitivity functions measured with prolonged retinal stabilization and the spatial characteristics of recorded eye movements. The Supplementary Methods section provides further details about the retinal stabilization technique used in the experiments. (PDF 248 kb)
This file contains Supplementary Video 1 which is a reconstruction of the visual input to the retina during a trial of Experiment 1. For clarity, the stimulus has been enlarged by elimination of the Gaussian window. The modulations resulting from fixational eye movements enhance the high-frequency grating. See Supplementary Video Legend for detail. (MOV 88 kb)
This file contains Supplementary Video 2 which is a reconstruction of the visual input to the retina during a trial of Experiment 1. For clarity, the stimulus has been enlarged by elimination of the Gaussian window. The modulations resulting from fixational eye movements enhance the high-frequency grating. See Supplementary Video Legend for detail. (MOV 87 kb)
This file contains Supplementary Video 3 which is a reconstruction of the visual input to the retina during a trial of Experiment 2. For clarity, the stimulus has been enlarged by elimination of the Gaussian window. The modulations resulting from fixational eye movements attenuate the low-frequency grating. See Supplementary Video Legend for detail. (MOV 147 kb)
This file contains Supplementary Video 4 which is a reconstruction of the visual input to the retina during a trial of Experiment 2. For clarity, the stimulus has been enlarged by elimination of the Gaussian window. The modulations resulting from fixational eye movements attenuate the low-frequency grating. See Supplementary Video Legend for detail. (MOV 156 kb)
This file contains Supplementary Video 5 which is areconstruction of the visual input to the retina during a fixation on a natural image. The modulations resulting from fixational eye movements enhance high spatial frequencies and attenuate low spatial frequencies. See Supplementary Video Legend for detail. (MOV 119 kb)
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Rucci, M., Iovin, R., Poletti, M. et al. Miniature eye movements enhance fine spatial detail. Nature 447, 852–855 (2007). https://doi.org/10.1038/nature05866
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