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Microsaccades precisely relocate gaze in a high visual acuity task

Abstract

The image on the retina is never stationary. Microscopic relocations of gaze, known as microsaccades, occur even during steady fixation. It has long been thought that microsaccades enable exploration of small regions in the scene in the same way saccades are normally used to scan larger regions. This hypothesis, however, has remained controversial, as it is believed that microsaccades are suppressed during fine spatial judgments. We examined the eye movements of human observers in a high-acuity visuomotor task, the threading of a needle in a computer-simulated virtual environment. Using a method for gaze-contingent display that enables accurate localization of the line of sight, we found that microsaccades precisely move the eye to nearby regions of interest and are dynamically modulated by the ongoing demands of the task. These results indicate that microsaccades are part of the oculomotor strategy by which the visual system acquires fine spatial detail.

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Figure 1: Threading a virtual needle.
Figure 2: Comparison of saccade characteristics in three different tasks: threading, sustained fixation on a marker and free viewing of natural images.
Figure 3: Modulation of saccade characteristics.
Figure 4: Analysis of fixation locations.
Figure 5: Analysis of microsaccades.
Figure 6: Interaction between microsaccades and corrections in the thread-needle alignment.

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References

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

    Article  CAS  Google Scholar 

  2. Collewijn, H. & Kowler, E. The significance of microsaccades for vision and oculomotor control. J. Vis. 8, 1–21 (2008).

    Article  Google Scholar 

  3. Rolfs, M. Microsaccades: Small steps on a long way. Vision Res. 49, 2415–2441 (2009).

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  5. Ditchburn, R.W., Fender, D.H. & Mayne, S. Vision with controlled movements of the retinal image. J. Physiol. (Lond.) 145, 98–107 (1959).

    Article  CAS  Google Scholar 

  6. 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 

  7. Cornsweet, T.N. Determination of the stimuli for involuntary drifts and saccadic eye movements. J. Opt. Soc. Am. 46, 987–993 (1956).

    Article  CAS  Google Scholar 

  8. Engbert, R. & Kliegl, R. Microsaccades keep the eyes' balance during fixation. Psychol. Sci. 15, 431–436 (2004).

    Article  Google Scholar 

  9. Cunitz, R.J. & Steinman, R.M. Comparison of saccadic eye movements during fixation and reading. Vision Res. 9, 683–693 (1969).

    Article  CAS  Google Scholar 

  10. Winterson, B.J. & Collewijn, H. Microsaccades during finely guided visuomotor tasks. Vision Res. 16, 1387–1390 (1976).

    Article  CAS  Google Scholar 

  11. Bridgeman, B. & Palca, J. The role of microsaccades in high acuity observational tasks. Vision Res. 20, 813–817 (1980).

    Article  CAS  Google Scholar 

  12. 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  CAS  Google Scholar 

  13. Poletti, M. & Rucci, M. Fixational eye movements under various conditions of image fading. J. Vis. 10, 1–18 (2010).

    Article  Google Scholar 

  14. Santini, F., Redner, G., Iovin, R. & Rucci, M. EyeRIS: A general-purpose system for eye movement contingent display control. Behav. Res. Methods 39, 350–364 (2007).

    Article  Google Scholar 

  15. Rucci, M., Iovin, R., Poletti, M. & Santini, F. Miniature eye movements enhance fine spatial detail. Nature 447, 851–854 (2007).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  17. Ditchburn, R.W. & Ginsborg, B.L. Involuntary eye movements during fixation. J. Physiol. (Lond.) 119, 1–17 (1953).

    Article  CAS  Google Scholar 

  18. Putnam, N.M. et al. The locus of fixation and the foveal cone mosaic. J. Vis. 5, 632–639 (2005).

    Article  Google Scholar 

  19. Steinman, R.M. Effect of target size, luminance and color on monocular fixation. J. Opt. Soc. Am. 55, 1158–1165 (1965).

    Article  Google Scholar 

  20. Hafed, Z.M., Goffart, L. & Krauzlis, R. A neural mechanism for microsaccade generation in the primate superior colliculus. Science 323, 940–943 (2009).

    Article  CAS  Google Scholar 

  21. Timberlake, G.T., Wyman, D., Skavenski, A.A. & Steinman, R.M. The oculomotor error signal in the fovea. Vision Res. 12, 1059–1064 (1972).

    Article  CAS  Google Scholar 

  22. Haddad, G.M. & Steinman, R.M. The smallest voluntary saccade: Implications for fixation. Vision Res. 13, 1075–1086 (1973).

    Article  CAS  Google Scholar 

  23. Snodderly, D.M. Effects of light and dark environments on macaque and human fixational eye movements. Vision Res. 27, 401–415 (1987).

    Article  CAS  Google Scholar 

  24. Kagan, I., Gur, M. & Snodderly, D.M. Saccades and drifts differentially modulate neuronal activity in V1: effects of retinal image motion, position and extraretinal influences. J. Vis. 8, 1–25 (2008).

    Article  Google Scholar 

  25. Epelboim, J.L. et al. The function of visual search and memory in sequential looking tasks. Vision Res. 35, 3401–3422 (1995).

    Article  CAS  Google Scholar 

  26. Ballard, D.H., Hayhoe, M.M. & Pelz, J.B. Memory representations in natural tasks. J. Cogn. Neurosci. 7, 66–80 (1995).

    Article  CAS  Google Scholar 

  27. Land, M., Mennie, N. & Rusted, J. The roles of vision and eye movements in the control of activities of daily living. Perception 28, 1311–1328 (1999).

    Article  CAS  Google Scholar 

  28. Johansson, R.S., Westling, G., Bäckström, A. & Flanagan, J.R. Eye-hand coordination in object manipulation. J. Neurosci. 21, 6917–6932 (2001).

    Article  CAS  Google Scholar 

  29. Rucci, M. & Desbordes, G. Contributions of fixational eye movements to the discrimination of briefly presented stimuli. J. Vis. 3, 852–864 (2003).

    Article  Google Scholar 

  30. van Hateren, J.H. & Ruderman, D.L. Independent component analysis of natural image sequences yields spatio-temporal filters similar to simple cells in primary visual cortex. Proc. Biol. Sci. 265, 2315–2320 (1998).

    Article  CAS  Google Scholar 

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Acknowledgements

The authors thank A. Casile and D. Richters for helpful comments on the manuscript. This work was supported by a grant from the US National Institutes of Health (EY018363) and grants from the National Science Foundation (BCS-0719849 and IOS-0843304).

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Authors

Contributions

H.-K.K. and M.P. collected data. M.R. supervised the experiments. All of the authors contributed to the design of the experiments, data analysis and the writing of the manuscript. The first two authors contributed equally to this work.

Corresponding author

Correspondence to Michele Rucci.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Text and Figures

Supplementary Figure 1 and Supplementary Results (PDF 94 kb)

Supplementary Video 1

Example of experimental trial. Reconstruction of the stimulus experienced by the subject during an experimental trial. The blue cross marks the position of the current location of gaze, which has been superimposed to the stimulus in order to show the eye movements performed by the observer. This cross was not displayed during the actual experiment. Intervals in which the cross turns red represent periods of blink. (MOV 838 kb)

Supplementary Video 2

Example of experimental trial. Reconstruction of the stimulus experienced by the subject during an experimental trial. The blue cross marks the position of the current location of gaze, which has been superimposed to the stimulus in order to show the eye movements performed by the observer. This cross was not displayed during the actual experiment. Intervals in which the cross turns red represent periods of blink. (MOV 844 kb)

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Ko, Hk., Poletti, M. & Rucci, M. Microsaccades precisely relocate gaze in a high visual acuity task. Nat Neurosci 13, 1549–1553 (2010). https://doi.org/10.1038/nn.2663

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