Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

The role of fixational eye movements in visual perception

Nature Reviews Neuroscience volume 5, pages 229–240 (2004)Cite this article

Key Points

  • Fixational eye movements are small displacements of the eyeballs which ensure that vision does not fade during fixation. There are three classes — tremor (the smallest), drifts and microsaccades (the largest). Traditionally, fixational eye movements have been studied with retinal stabilization techniques.

  • The functional role of fixational eye movements in perception is controversial. Microsaccades have received the most attention, and there is evidence for and against their role in perception. However, the existence of microsaccade-related activity in the visual pathway indicates that they might be involved in perception.

  • Several studies have focused on unravelling the neural code of the responses elicited by the different fixational eye movements. Microsaccades have been most extensively studied. The burst-like nature of the activity elicited by microsaccades has attracted particular attention, but its physiological meaning remains uncertain.

  • Despite the existence of fixational eye movements, perception is stable. This fact has been explained by a hypothetical microsaccadic suppression mechanism, and several models for such a mechanism have been proposed. The underlying phenomena have yet to be discovered.

  • Fixational eye movements can be modulated by environmental (illumination conditions) and cognitive (attention) factors. Other phenomena also seem to exert a modulatory influence on these movements, but such factors need to be investigated.

  • Among the outstanding questions in this field are: which circuits control fixational eye movements; what is the neural basis of microsaccadic suppression; what are the mechanisms that underlie the effect of cognitive factors during fixation; and what is the meaning of the burst firing that is correlated with microsaccades?

Abstract

Our eyes continually move even while we fix our gaze on an object. Although these fixational eye movements have a magnitude that should make them visible to us, we are unaware of them. If fixational eye movements are counteracted, our visual perception fades completely as a result of neural adaptation. So, our visual system has a built-in paradox — we must fix our gaze to inspect the minute details of our world, but if we were to fixate perfectly, the entire world would fade from view. Owing to their role in counteracting adaptation, fixational eye movements have been studied to elucidate how the brain makes our environment visible. Moreover, because we are not aware of these eye movements, they have been studied to understand the underpinnings of visual awareness. Recent studies of fixational eye movements have focused on determining how visible perception is encoded by neurons in various visual areas of the brain.

This is a preview of subscription content, access via your institution

Relevant articles

Open Access articles citing this article.

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

Learn more

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Eye movements during visual fixation.
Figure 2: Early retinal stabilization studies.
Figure 3: Fixational eye movements carry the image across the retinal photoreceptors.
Figure 4: Fixational eye movements increase retinal activity.
Figure 5: Neural responses to microsaccades in the primate.

References

  1. Riggs, L. A. & Ratliff, F. The effects of counteracting the normal movements of the eye. J. Opt. Soc. Am. 42, 872–873 (1952). This classic paper, together with references 2 and 9, showed that when all eye movements are counteracted in the laboratory, visual perception rapidly fades owing to sensory adaptation.

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  3. Judge, S. J., Richmond, B. J. & Chu, F. C. Implantation of magnetic search coils for measurement of eye position: an improved method. Vision Res. 20, 535–538 (1980).

    Article  CAS  PubMed  Google Scholar 

  4. Hartline, H. K. The nerve messages in the fibers of the visual pathway. J. Opt. Soc. Am. 30, 239–247 (1940).

    Article  Google Scholar 

  5. Kuffler, S. W. Neurons in the retina: organization, inhibition and excitation problems. Cold Spring Harb. Symp. Quant. Biol. 17, 281–292 (1952).

    Article  CAS  PubMed  Google Scholar 

  6. Hubel, D. H. & Wiesel, T. N. Receptive fields and functional architecture in two non-striate visual areas (18 and 19) of the cat. J. Neurophysiol. 28, 229–289 (1965).

    Article  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  8. Skavenski, A. A., Hansen, R. M., Steinman, R. M. & Winterson, B. J. Quality of retinal image stabilization during small natural and artificial body rotations in man. Vision Res. 19, 675–683 (1979).

    Article  CAS  PubMed  Google Scholar 

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

    Book  Google Scholar 

  10. Krauskopf, J. Effect of retinal image motion on contrast thresholds for maintained vision. J. Opt. Soc. Am. 47, 740–744 (1957).

    Article  CAS  PubMed  Google Scholar 

  11. 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 

  12. Gerrits, H. J. & Vendrik, A. J. Artificial movements of a stabilized image. Vision Res. 10, 1443–1456 (1970).

    Article  CAS  PubMed  Google Scholar 

  13. Sharpe, C. R. The visibility and fading of thin lines visualized by their controlled movement across the retina. J. Physiol. (Lond.) 222, 113–134 (1972).

    Article  CAS  Google Scholar 

  14. Drysdale, A. E. The visibility of retinal blood vessels. Vision Res. 15, 813–818 (1975).

    Article  CAS  PubMed  Google Scholar 

  15. Gerrits, H. J., De Haan, B. & Vendrik, A. J. Experiments with retinal stabilized images. Relations between the observations and neural data. Vision Res. 6, 427–440 (1966).

    Article  CAS  PubMed  Google Scholar 

  16. Ratliff, F. Stationary retinal image requiring no attachments to the eye. J. Opt. Soc. Am. 48, 274–275 (1958).

    Article  Google Scholar 

  17. Coppola, D. & Purves, D. The extraordinarily rapid disappearance of entoptic images. Proc. Natl Acad. Sci. USA 93, 8001–8004 (1996). This study showed that visual fading due to retinal stabilization can happen extremely quickly, in less than 80 ms. This fast fading of retinal images in the absence of eye movements has made the field reconsider the dynamics of neural adaptation during normal vision.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Kelly, D. H. New method of stabilizing retinal images. J. Opt. Soc. Am. 65, 1184 (1975).

    Article  Google Scholar 

  19. Gur, M. & Snodderly, D. M. Studying striate cortex neurons in behaving monkeys: benefits of image stabilization. Vision Res. 27, 2081–2087 (1987).

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  21. Pritchard, R. M. Stabilized images on the retina. Sci. Am. 204, 72–78 (1961).

    Article  CAS  PubMed  Google Scholar 

  22. Barlow, H. B. Slippage of contact lenses and other artifacts in relation to fading and regeneration of supposedly stable retinal images. Q. J. Exp. Psychol. 15, 36–51 (1963).

    Article  Google Scholar 

  23. Helmholtz, H. Helmholtz's Treatise on Physiological Optics (ed. Southall, J. P. C.) (Gryphon Editions, Birmingham, 1985).

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  25. Carpenter, R. H. S. Movements of the Eyes (Pion, London, 1988).

    Google Scholar 

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

    Article  Google Scholar 

  27. Spauschus, A., Marsden, J., Halliday, D. M., Rosenberg, J. R. & Brown, P. The origin of ocular microtremor in man. Exp. Brain Res. 126, 556–562 (1999).

    Article  CAS  PubMed  Google Scholar 

  28. Greschner, M., Bongard, M., Rujan, P. & Ammermuller, J. Retinal ganglion cell synchronization by fixational eye movements improves feature stimation. Nature 5, 341–347 (2002). Ganglion neurons from the turtle retina were stimulated by stimuli that moved in a fashion that simulated eye movements during fixation. Fixational eye movements not only led to increased activity of isolated retinal ganglion neurons, but also to increased synchronization in the retinal ganglion cell network.

    CAS  Google Scholar 

  29. Martinez-Conde, S., Macknik, S. L. & Hubel, D. H. The function of bursts of spikes during visual fixation in the awake primate lateral geniculate nucleus and primary visual cortex. Proc. Natl Acad. Sci. USA 99, 13920–13925 (2002). The parameters of bursts of spikes following microsaccades in the lateral geniculate nucleus and in area V1 depend on whether the visual stimuli presented are optimal or non-optimal for each of these areas.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Riggs, L. A. & Ratliff, F. Visual acuity and the normal tremor of the eyes. Science 114, 17–18 (1951).

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  33. Nachmias, J. Two-dimensional motion of the retinal image during monocular fixation. J. Opt. Soc. Am. 49, 901–908 (1959).

    Article  CAS  PubMed  Google Scholar 

  34. Nachmias, J. Determiners of the drift of the eye during monocular fixation. J. Opt. Soc. Am. 51, 761–766 (1961).

    Article  CAS  PubMed  Google Scholar 

  35. 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  PubMed  Google Scholar 

  36. St Cyr, G. J. & Fender, D. H. The interplay of drifts and flicks in binocular fixation. Vision Res. 9, 245–265 (1969).

    Article  CAS  PubMed  Google Scholar 

  37. Krauskopf, J., Cornsweet, T. N. & Riggs, L. A. Analysis of eye movements during monocular and binocular fixation. J. Opt. Soc. Am. 50, 572–578 (1960).

    Article  CAS  PubMed  Google Scholar 

  38. Eizenman, M., Hallett, P. E. & Frecker, R. C. Power spectra for ocular drift and tremor. Vision Res. 25, 1635–1640 (1985).

    Article  CAS  PubMed  Google Scholar 

  39. Shakhnovich, A. R. & Thomas, J. G. Micro-tremor of the eyes of comatose patients. Electroencephalogr. Clin. Neurophysiol. 42, 117–119 (1977).

    Article  CAS  PubMed  Google Scholar 

  40. 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). Fixational microsaccades during the presentation of stationary stimuli led to increases in the activity of primate area V1 neurons. Increases in neural firing after microsaccades were clumped in bursts of spikes.

    Article  CAS  PubMed  Google Scholar 

  41. Ditchburn, R. W. The function of small saccades. Vision Res. 20, 271–272 (1980).

    Article  CAS  PubMed  Google Scholar 

  42. Horwitz, G. D. & Albright, T. D. Short-latency fixational saccades induced by luminance increments. J. Neurophysiol. 90, 1333–1339 (2003).

    Article  PubMed  Google Scholar 

  43. Skavenski, A. A., Robinson, D. A., Steinman, R. M. & Timberlake, G. T. Miniature eye movements of fixation in rhesus monkey. Vision Res. 15, 1269–1273 (1975).

    Article  CAS  PubMed  Google Scholar 

  44. Snodderly, D. M. & Kurtz, D. Eye position during fixation tasks: comparison of macaque and human. Vision Res. 25, 83–98 (1985).

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  46. Fiorentini, A. & Ercoles, A. M. Involuntary eye movements during attempted monocular fixation. Atti Fond. Giorgio Ronchi 21, 199–217 (1966).

    Google Scholar 

  47. Engbert, R. & Kliegl, R. Microsaccades keep the eyes' balance during fixation. Psychol. Sci. (in the press)

  48. Zuber, B. L. & Stark, L. Microsaccades and the velocity–amplitude relationship for saccadic eye movements. Science 150, 1459–1460 (1965). This classic study showed a linear relationship between microsaccade amplitudes and velocities. This followed the extrapolation of the same relationship for large saccades, and indicated that both large saccades and microsaccades might be generated by the same neural mechanisms.

    Article  CAS  PubMed  Google Scholar 

  49. Moller, F., Laursen, M. L., Tygesen, J. & Sjolie, A. K. Binocular quantification and characterization of microsaccades. Graefes Arch. Clin. Exp. Ophthalmol. 240, 765–770 (2002).

    Article  CAS  PubMed  Google Scholar 

  50. Wurtz, R. H. Vision for the control of movement. The Friedenwald Lecture. Invest. Ophthalmol. Vis. Sci. 37, 2130–2145 (1996).

    CAS  PubMed  Google Scholar 

  51. Sparks, D. L. The brainstem control of saccadic eye movements. Nature Rev. Neurosci. 3, 952–964 (2002).

    Article  CAS  Google Scholar 

  52. Lord, M. P. Measurement of binocular eye movements of subjects in the sitting position. Brit. J. Ophthal. 35, 21–30 (1951).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Engbert, R. & Kliegl, R. in The Mind's Eyes: Cognitive and Applied Aspects of Eye Movements (eds Hyona, J., Radach, R. & Deubel, H.) 103–117 (Elsevier, Oxford, 2003).

    Book  Google Scholar 

  54. Westheimer, G. The spatial sense of the eye. Proctor lecture. Invest. Ophthalmol. Vis. Sci. 18, 893–912 (1979).

    CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  57. Kowler, E. & Steinman, R. M. The role of small saccades in counting. Vision Res. 17, 141–146 (1977).

    Article  CAS  PubMed  Google Scholar 

  58. Kowler, E. & Steinman, R. M. Miniature saccades: eye movements that do not count. Vision Res. 19, 105–108 (1979).

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  60. Kowler, E. & Steinman, R. M. Small saccades serve no useful purpose: reply to a letter by R. W. Ditchburn. Vision Res. 20, 273–276 (1980).

    Article  CAS  PubMed  Google Scholar 

  61. Livingstone, M. S., Freeman, D. C. & Hubel, D. H. Visual responses in V1 of freely viewing monkeys. Cold Spring Harb. Symp. Quant. Biol. 61, 27–37 (1996).

    Article  CAS  PubMed  Google Scholar 

  62. Macknik, S. L. & Livingstone, M. S. Neuronal correlates of visibility and invisibility in the primate visual system. Nature Neurosci. 1, 144–149 (1998).

    Article  CAS  PubMed  Google Scholar 

  63. Gur, M., Beylin, A. & Snodderly, D. M. Response variability of neurons in primary visual cortex (V1) of alert monkeys. J. Neurosci. 17, 2914–2920 (1997).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Gur, M. & Snodderly, D. M. Visual receptive fields of neurons in primary visual cortex (V1) move in space with the eye movements of fixation. Vision Res. 37, 257–265 (1997).

    Article  CAS  PubMed  Google Scholar 

  65. Bair, W. & O'Keefe, L. P. The influence of fixational eye movements on the response of neurons in area MT of the macaque. Vis. Neurosci. 15, 779–786 (1998).

    Article  CAS  PubMed  Google Scholar 

  66. 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  PubMed  Google Scholar 

  67. 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  PubMed  Google Scholar 

  68. Reppas, J. B., Usrey, W. M. & Reid, R. C. Saccadic eye movements modulate visual responses in the lateral geniculate nucleus. Neuron 35, 961–974 (2002).

    Article  CAS  PubMed  Google Scholar 

  69. Hafed, Z. M. & Clark, J. J. Microsaccades as an overt measure of covert attention shifts. Vision Res. 42, 2533–2545 (2002). This study, together with references 70 and 72, comprised the first systematic attempts to characterize the influence of cognition on the dynamics of fixational eye movements. These studies provided a rich basis for what is likely to become a lively field of enquiry.

    Article  PubMed  Google Scholar 

  70. Engbert, R. & Kliegl, R. Microsaccades uncover the orientation of covert attention. Vision Res. 43, 1035–1045 (2003).

    Article  PubMed  Google Scholar 

  71. Rolfs, M., Engbert, R. & Kliegl, R. Microsaccade orientation supports attentional enhancement opposite to a peripheral cue: commentary on Tse, Sheinberg, and Logothetis. Psychol. Sci. (in the press).

  72. Tse, P. U., Sheinberg, D. L. & Logothetis, N. K. Fixational eye movements are not affected by abrupt onsets that capture attention. Vision Res. 42, 1663–1669 (2002).

    Article  CAS  PubMed  Google Scholar 

  73. Tse, P. U., Sheinberg, D. S. & Logothetis, N. K. The distribution of microsaccade directions need not reveal the location of attention. Psychol. Sci. (in the press).

  74. Gerrits, H. J. & Vendrik, A. J. The influence of stimulus movements on perception in parafoveal stabilized vision. Vision Res. 14, 175–180 (1974).

    Article  CAS  PubMed  Google Scholar 

  75. Clowes, M. B. A note on colour discrimination under conditions of retinal image constraint. Opt. Acta (Lond.) 9, 65–68 (1962).

    Article  CAS  Google Scholar 

  76. Macknik, S. L., Martinez-Conde, S. & Haglund, M. M. The role of spatiotemporal edges in visibility and visual masking. Proc. Natl Acad. Sci. USA 97, 7556–7560 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Leopold, D. A. & Logothetis, N. K. Activity changes in early visual cortex reflect monkeys percepts during binocular rivalry. Nature 379, 549–553 (1996).

    Article  CAS  PubMed  Google Scholar 

  78. Albrecht, D. G. & Hamilton, D. B. Striate cortex of monkey and cat: contrast response function. J. Neurophysiol. 48, 217–237 (1982).

    Article  CAS  PubMed  Google Scholar 

  79. Albrecht, D. G. Visual cortex neurons in monkey and cat: effect of contrast on the spatial and temporal phase transfer functions. Vis. Neurosci. 12, 1191–1210 (1995).

    Article  CAS  PubMed  Google Scholar 

  80. Gawne, T. J., Kjaer, T. W. & Richmond, B. J. Latency: another potential code for feature binding in striate cortex. J. Neurophysiol. 76, 1356–1360 (1996).

    Article  CAS  PubMed  Google Scholar 

  81. Usrey, W. M., Reppas, J. B. & Reid, R. C. Paired-spike interactions and synaptic efficacy of retinal inputs to the thalamus. Nature 395, 384–387 (1998).

    Article  CAS  PubMed  Google Scholar 

  82. Kara, P. & Reid, R. C. Efficacy of retinal spikes in driving cortical responses. J. Neurosci. 23, 8547–8557 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Bridgeman, B. B. & Macknik, S. L. Saccadic suppression relies on luminance information. Psychol. Res. 58, 163–168 (1995).

    Article  CAS  PubMed  Google Scholar 

  84. Macknik, S. L., Fisher, B. D. & Bridgeman, B. Flicker distorts visual space constancy. Vision Res. 31, 2057–2064 (1991).

    Article  CAS  PubMed  Google Scholar 

  85. Wurtz, R. H. Visual cortex neurons: response to stimuli during rapid eye movements. Science 162, 1148–1150 (1968).

    Article  CAS  PubMed  Google Scholar 

  86. Wurtz, R. H. Comparison of effects of eye movements and stimulus movements on striate cortex neurons of the monkey. J. Neurophysiol. 32, 987–994 (1969).

    Article  CAS  PubMed  Google Scholar 

  87. Ross, J., Morrone, M. C., Goldberg, M. E. & Burr, D. C. Changes in visual perception at the time of saccades. Trends Neurosci. 24, 113–121 (2001).

    Article  CAS  PubMed  Google Scholar 

  88. Beeler, G. W. Visual threshold changes resulting from spontaneous saccadic eye movements. Vision Res. 7, 769–775 (1967).

    Article  PubMed  Google Scholar 

  89. Krauskopf, J. Lack of inhibition during involuntary saccades. Am. J. Psychol. 79, 73–81 (1966).

    Article  Google Scholar 

  90. Sperling, G. in Eye Movements and Their Role in Visual and Cognitive Processes (ed. Kowler, E.) 307–351 (Elsevier, Amsterdam, 1990).

    Google Scholar 

  91. Rucci, M., Edelman, G. E. & Wray, J. Modeling LGN responses dring free-viewing: a possible role of microscopic eye movements in the refinement of cortical orientation selectivity. J. Neurosci. 20, 4708–4720 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  93. Masland, R. H. The retina's fancy tricks. Nature 423, 387 (2003).

    Article  CAS  PubMed  Google Scholar 

  94. Zuber, B. L., Crider, A. & Stark, L. Saccadic suppression associated with microsaccades. Q. Prog. Rep. 74, 244–249 (1964).

    Google Scholar 

  95. Zuber, B. L. & Stark, L. Saccadic suppression: elevation of visual threshold associated with saccadic eye movements. Exp. Neurol. 16, 65–79 (1966).

    Article  CAS  PubMed  Google Scholar 

  96. Murakami, I. & Cavanagh, P. A jitter after-effect reveals motion-based stabilization of vision. Nature 395, 798–801 (1998). A striking visual illusion that showed how jittery our perception of the world would be if fixational eye movements were not systematically compensated for by the visual system.

    Article  CAS  PubMed  Google Scholar 

  97. Murakami, I. & Cavanagh, P. Visual jitter: evidence for visual-motion-based compensation of retinal slip due to small eye movements. Vision Res. 41, 173–186 (2001).

    Article  CAS  PubMed  Google Scholar 

  98. Sasaki, Y., Murakami, I., Cavanagh, P. & Tootell, R. H. Human brain activity during illusory visual jitter as revealed by functional magnetic resonance imaging. Neuron 35, 1147–1156 (2002).

    Article  CAS  PubMed  Google Scholar 

  99. Barash, S., Melikyan, A., Sivakov, A. & Tauber, M. Shift of visual fixation dependent on background illumination. J. Neurophysiol. 79, 2766–2781 (1998).

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  101. Fender, D. H. Variation of fixation direction with colour of fixation target. Br. J. Ophthalmol. 39, 294–297 (1955).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Sansbury, R. V., Skavenski, A. A., Haddad, G. M. & Steinman, R. M. Normal fixation of eccentric targets. J. Opt. Soc. Am. 63, 612–614 (1973).

    Article  CAS  PubMed  Google Scholar 

  103. Corbetta, M. et al. A common network of functional areas for attention and eye movements. Neuron 21, 761–773 (1998). This imaging study showed extensive anatomical overlap between the attentional and eye-movement related areas of the brain.

    Article  CAS  PubMed  Google Scholar 

  104. Barlow, H. B. Eye movements during fixation. J. Physiol. (Lond.) 116, 290–306 (1952).

    Article  CAS  Google Scholar 

  105. Kowler, E. & Steinman, R. M. The effect of expectations on slow oculomotor control. I. Periodic target steps. Vision Res. 19, 619–632 (1979).

    Article  CAS  PubMed  Google Scholar 

  106. Troxler, D. in Ophthalmologische Bibliothek (eds Himly, K. & Schmidt, J. A.) 1–53 (Springer, Jena, 1804).

    Google Scholar 

  107. Clarke, F. J. J. Rapid light adaptation of localised areas of the extra-foveal retina. Opt. Acta (Lond.) 4, 69–77 (1957).

    Article  Google Scholar 

  108. Clarke, F. J. J. A study of Troxler's effect. Opt. Acta (Lond.) 7, 219–236 (1960).

    Article  Google Scholar 

  109. Clarke, F. J. J. Visual recovery following local adaptation of the perpheral retina (Troxler's effect). Opt. Acta (Lond.) 8, 121–135 (1961).

    Article  Google Scholar 

  110. Clarke, F. J. J. & Belcher, S. J. On the localization of Troxler's effect in the visual pathway. Vision Res. 2, 53–68 (1962).

    Article  Google Scholar 

  111. Gilchrist, I. D., Brown, V. & Findlay, J. M. Saccades without eye movements. Nature 390, 130–131 (1997).

    Article  CAS  PubMed  Google Scholar 

  112. Gilchrist, I. D., Brown, V., Findlay, J. M. & Clarke, M. P. Using the eye-movement system to control the head. Proc. R. Soc. Lond. B 265, 1831–1836 (1998).

    Article  CAS  Google Scholar 

  113. Land, M. F., Furneaux, S. M. & Gilchrist, I. D. The organization of visually mediated actions in a subject without eye movements. Neurocase 8, 80–87 (2002).

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  115. Verheijen, F. J. A simple after image method demonstrating the involuntary multidirectional eye movements during fixation. Opt. Acta (Lond.) 8, 309–312 (1961).

    Article  CAS  Google Scholar 

  116. Simon, F., Schulz, E., Rassow, B. & Haase, W. Binocular micromovement recording of human eyes:—methods. Graefes Arch. Clin. Exp. Ophthalmol. 221, 293–298 (1984).

    Article  CAS  PubMed  Google Scholar 

  117. Riggs, L. A., Armington, J. C. & Ratliff, F. Motions of the retinal image during fixation. J. Opt. Soc. Am. 44, 315–321 (1954).

    Article  CAS  PubMed  Google Scholar 

  118. Adler, F. H. & Fliegelman, M. Influence of fixation on the visual acuity. Arch. Ophthalmol. 12, 475–483 (1934).

    Article  Google Scholar 

  119. Schulz, E. Binocular micromovements in normal persons. Graefes Arch. Clin. Exp. Ophthalmol. 222, 95–100 (1984).

    Article  CAS  PubMed  Google Scholar 

  120. Srebro, R. Fixation of normal and amblyopic eyes. Arch. Ophthalmol. 101, 214–217 (1983).

    Article  CAS  PubMed  Google Scholar 

  121. West, D. C. & Boyce, P. R. The effect of flicker on eye movement. Vision Res. 8, 171–192 (1968).

    Article  CAS  PubMed  Google Scholar 

  122. Boyce, P. R. Monocular fixation in human eye movement. Proc. R. Soc. Lond. B 167, 293–315 (1967).

    Article  CAS  PubMed  Google Scholar 

  123. Malinov, I. V., Epelboim, J., Herst, A. N. & Steinman, R. M. Characteristics of saccades and vergence in two types of sequential looking tasks. Vision Res. 40, 2083–2090 (2000).

    Article  CAS  PubMed  Google Scholar 

  124. Kingstone, A., Fendrich, R., Wessinger, C. M. & Reuter-Lorenz, P. A. Are microsaccades responsible for the gap effect? Percept. Psychophys. 57, 796–801 (1995).

    Article  CAS  PubMed  Google Scholar 

  125. Sabrin, H. W. & Kertesz, A. E. Microsaccadic eye movements and binocular rivalry. Percept. Psychophys. 28, 150–154 (1980).

    Article  CAS  PubMed  Google Scholar 

  126. Lord, M. P. & Wright, W. D. Eye movements during monocular fixation. Nature 162, 25–26 (1948).

    Article  CAS  PubMed  Google Scholar 

  127. Ditchburn, R. W. & Foley-Fisher, J. A. Assembled data in eye movements. Opt. Acta (Lond.) 14, 113–118 (1967).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank Y. Duran for technical assistance and X. G. Troncoso for comments on the manuscript. This study was funded by the Barrow Neurological Foundation and the National Eye Institute.

Author information

Authors and Affiliations

  1. Barrow Neurological Institute, St. Joseph's Hospital, 350 W. Thomas Road, Phoenix, 85013, Arizona, USA

    Susana Martinez-Conde & Stephen L. Macknik

  2. Department of Neurobiology, Harvard Medical School, 220 Longwood Avenue, Boston, 02115, Massachusetts, USA

    David H. Hubel

Authors
  1. Susana Martinez-Conde
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Stephen L. Macknik
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. David H. Hubel
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Susana Martinez-Conde.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Related links

Related links

FURTHER INFORMATION

An online algorithm for microsaccade detection

Fading dot demonstration

Shimmer demonstration

Susana Martinez-Conde's page

Troxler studies

Visual jitter demonstration

Glossary

ENTOPTIC STRUCTURES

Structures within the eye. When these become visible they give rise to entoptic images.

NYSTAGMUS

Involuntary rhythmical oscillations of one or both eyes.

FOVEA

The retinal region with maximal concentration of photoreceptors, where visual acuity is highest.

FLICKER FUSION THRESHOLD

The rate of flicker at which the flickering stimulus being viewed appears non-flickering (approximately 50–60 Hz in humans).

CONJUGATE

Coordinated in the two eyes.

MAIN SEQUENCE

The linear correlation between saccadic speed and amplitude.

RECEPTIVE FIELD

The area of the sensory space in which stimulus presentation leads to the response of a particular sensory neuron.

BINOCULAR DISPARITY

The difference in gaze position of the two eyes that gives rise to stereovision.

VISUAL MASKING

An illusion in which a normally visible target object is rendered invisible by a mask object.

NEURAL CODE

The language, expressed as a pattern of neuronal impulses, that neurons use to send information to each other.

EXTRARETINAL ACTIVATION

Responses in the visual system that occur in the absence of visual stimuli (such as one might see due to feedback from motor areas).

SPATIAL SUMMATION

The way in which non-overlapping retinal stimulation is integrated within dendrites to produce a stronger neuronal response.

BURSTS

Clusters of action potentials.

TEMPORAL SUMMATION

The way in which non-simultaneous synaptic events combine in time. One of the basic elements of synaptic integration.

LONG, TIGHT BURST

A type of burst consisting of a large number of spikes that occur in rapid succession.

SCOTOPIC CONDITIONS

Dim light conditions in which only the rods of the retina are active.

PHOTOPIC CONDITIONS

Bright light conditions in which only the cones of the retina are active.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Martinez-Conde, S., Macknik, S. & Hubel, D. The role of fixational eye movements in visual perception. Nat Rev Neurosci 5, 229–240 (2004). https://doi.org/10.1038/nrn1348

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1038/nrn1348

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing