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Miniature eye movements enhance fine spatial detail

Nature volume 447, pages 852–855 (2007)Cite this article

Abstract

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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Figure 1: Impact of retinal stabilization.
Figure 2: Contrast thresholds.
Figure 3: Controlled retinal image motion.
Figure 4: Influence of fixational eye movements on visual input.

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References

  1. Ratliff, F. & Riggs, L. A. Involuntary motions of the eye during monocular fixation. J. Exp. Psychol. 40, 687–701 (1950)

    Article  CAS  Google Scholar 

  2. Ditchburn, R. W. Eye movements in relation to retinal action. Opt. Acta 1, 171–176 (1955)

    Article  Google Scholar 

  3. Steinman, R. M., Haddad, G. M., Skavenski, A. A. & Wyman, D. Miniature eye movement. Science 181, 810–819 (1973)

    Article  ADS  CAS  Google Scholar 

  4. Murakami, I. & Cavanagh, P. A jitter after-effect reveals motion-based stabilization of vision. Nature 395, 798–801 (1998)

    Article  ADS  CAS  Google Scholar 

  5. Ditchburn, R. W. & Ginsborg, B. L. Vision with a stabilized retinal image. Nature 170, 36–37 (1952)

    Article  ADS  CAS  Google Scholar 

  6. Riggs, L. A. & Ratliff, F. The effects of counteracting the normal movements of the eye. J. Opt. Soc. Am. 42, 872–873 (1952)

    Google Scholar 

  7. Riggs, L. A., Ratliff, F., Cornsweet, J. C. & Cornsweet, T. N. The disappearance of steadily fixated visual test objects. J. Opt. Soc. Am. 43, 495–501 (1953)

    Article  ADS  CAS  Google Scholar 

  8. Yarbus, A. L. Eye Movements and Vision (Plenum, New York, 1967)

    Book  Google Scholar 

  9. Martinez-Conde, S., Macknik, S. L., Troncoso, X. G. & Dyar, T. A. Microsaccades counteract fading during fixation. Neuron 49, 297–305 (2006)

    Article  CAS  Google Scholar 

  10. Hering, E. Über die Grenzen der Sehschärfe. Berichte der Königlichen Sächsischen Gesellshaft der Wissenschaften. Math. Phys. Klasse 20, 16–24 (1899)

    Google Scholar 

  11. Averill, H. I. & Weymouth, F. W. Visual perception and the retinal mosaic, II. The influence of eye movements on the displacement threshold. J. Comp. Psychol. 5, 147–176 (1925)

    Article  Google Scholar 

  12. Marshall, W. H. & Talbot, S. A. in Biological Symposia——Visual Mechanisms. Vol. 7 (ed. Kluver, H.) 117–164 (Cattel, Lancaster, Pennsylvania, 1942)

    Google Scholar 

  13. Arend, L. E. Spatial differential and integral operations in human vision: implications of stabilized retinal image fading. Psychol. Rev. 80, 374–395 (1973)

    Article  Google Scholar 

  14. Ahissar, E. & Arieli, A. Figuring space by time. Neuron 32, 185–201 (2001)

    Article  CAS  Google Scholar 

  15. Greschner, M., Bongard, M., Rujan, P. & Ammermüller, J. Retinal ganglion cell synchronization by fixational eye movements improves feature estimation. Nature Neurosci. 5, 341–347 (2002)

    Article  CAS  Google Scholar 

  16. Ölveczky, B. P., Baccus, S. A. & Meister, M. Segregation of object and background motion in the retina. Nature 423, 401–408 (2003)

    Article  ADS  Google Scholar 

  17. Rucci, M. & Casile, A. Fixational instability and natural image statistics: implications for early visual representations. Network Comp. Neur. Syst. 16, 121–138 (2005)

    Article  Google Scholar 

  18. Santini, F., Redner, G., Iovin, R. & Rucci, M. EyeRIS: A general-purpose system for eye movement contingent display control. Behav. Res. Methods (in the press)

  19. Koenderink, J. J. Contrast enhancement and the negative afterimage. J. Opt. Soc. Am. A 62, 685–689 (1972)

    Article  ADS  CAS  Google Scholar 

  20. Kelly, D. H. Motion and vision. I. Stabilized images of stationary gratings. J. Opt. Soc. Am. 69, 1266–1274 (1979)

    Article  ADS  CAS  Google Scholar 

  21. Tulunay-Keesey, Ü. Fading of stabilized retinal images. J. Opt. Soc. Am. 72, 440–447 (1982)

    Article  ADS  CAS  Google Scholar 

  22. Tulunay-Keesey, Ü. & Jones, R. M. The effect of micromovements of the eye and exposure duration on contrast sensitivity. Vision Res. 16, 481–488 (1976)

    Article  CAS  Google Scholar 

  23. Steinman, R. M., Cunitz, R. J., Timberlake, G. T. & Herman, M. Voluntary control of microsaccades during maintained monocular fixation. Science 155, 1577–1579 (1967)

    Article  ADS  CAS  Google Scholar 

  24. Steinman, R. M. & Collewijn, H. Binocular retinal image motion during active head rotation. Vision Res. 20, 415–429 (1980)

    Article  CAS  Google Scholar 

  25. Kapoula, Z. A., Robinson, D. A. & Hain, T. C. Motion of the eye immediately after a saccade. Exp. Brain Res. 61, 386–394 (1986)

    Article  CAS  Google Scholar 

  26. Field, D. J. Relations between the statistics of natural images and the response properties of cortical cells. J. Opt. Soc. Am. A 4, 2379–2394 (1987)

    Article  ADS  CAS  Google Scholar 

  27. Leopold, D. A. & Logothetis, N. K. Microsaccades differentially modulate neural activity in the striate and extrastriate visual cortex. Exp. Brain Res. 123, 341–345 (1998)

    Article  CAS  Google Scholar 

  28. Martinez-Conde, S., Macknik, S. L. & Hubel, D. H. Microsaccadic eye movements and firing of single cells in the striate cortex of macaque monkeys. Nature Neurosci. 3, 251–258 (2000)

    Article  CAS  Google Scholar 

  29. Snodderly, D. M., Kagan, I. & Gur, M. Selective activation of visual cortex neurons by fixational eye movements: implications for neural coding. Vis. Neurosci. 18, 259–277 (2001)

    Article  CAS  Google Scholar 

  30. Macmillan, N. A. & Creelman, C. D. Detection Theory—A User’s Guide 2nd edn (L.Erlbaum Associates, London, 2005)

    Google Scholar 

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Acknowledgements

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.

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Authors and Affiliations

  1. Department of Cognitive and Neural Systems, Boston University, Boston, Massachusetts 02215, USA,

    Michele Rucci, Ramon Iovin, Martina Poletti & Fabrizio Santini

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  1. Michele Rucci
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  2. Ramon Iovin
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  4. Fabrizio Santini
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Corresponding author

Correspondence to Michele Rucci.

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Supplementary information

Supplementary Information

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)

Supplementary Video

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)

Supplementary Video

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)

Supplementary Video

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)

Supplementary Video

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)

Supplementary Video

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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