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Fixational Eye Movements

  • Robert G. AlexanderEmail author
  • Susana Martinez-Conde
Chapter
Part of the Studies in Neuroscience, Psychology and Behavioral Economics book series (SNPBE)

Abstract

There is too much going on around us to see everything at once, or to simultaneously process all the information in our field of view. Instead, we normally direct our gaze to parts of the scene that are particularly meaningful or important. Yet, even when we think that we are keeping our eyes still on an object of interest, our eyes remain in continuous motion. This chapter reviews the different kinds of “fixational” eye movements (the eye movements that occur when our gaze is “fixed” on an object or a point in space). We also discuss the effects that fixational eye movements have on vision and perception, their potential adaptive advantages, and their generation mechanisms. After reading this chapter, you will be able to articulate the importance of fixational eye movements in facilitating and influencing visual perception (for instance, in helping us to see the world and assisting us as we perform specific tasks). You will be able to explain the role of microsaccades (the largest of these small fixational eye movements) in counteracting neural adaptation and visual fading (the perceptual vanishing of an unchanging stimulus). You will also be able to outline the neural generation of microsaccades. In addition, this chapter will help you understand the relationship between fixational eye movements and shifts of attention. Finally, you will be able to describe, in general terms, the potential relevance of fixational eye movements to the diagnosis of neurological disorders.

Notes

Acknowledgements

This work was supported by a challenge grant from Research to Prevent Blindness Inc. to the Department of Ophthalmology at SUNY Downstate, the Empire Innovation Program (Award to SMC), and the National Science Foundation (Award 1734887). We thank Max Dorfman for his comments and Daniel Cortes-Rastrollo for administrative assistance.

Bibliography

  1. Abadi, R. V., & Gowen, E. (2004). Characteristics of saccadic intrusions. Vision Research, 44(23), 2675–2690.CrossRefPubMedGoogle Scholar
  2. Adler, F. H., & Fliegelman, M. (1934). Influence of fixation on the visual acuity. Archives of Ophthalmology, 12, 475–483.CrossRefGoogle Scholar
  3. Ahissar, E., & Arieli, A. (2012). Seeing via miniature eye movements: A dynamic hypothesis for vision. Frontiers in computational neuroscience, 6.Google Scholar
  4. Alexander, R. G., Macknik, S. L., & Martinez-Conde, S. (2018). Microsaccade characteristics in neurological and ophthalmic disease. Frontiers in Neurology, 9(144), 1–9.  https://doi.org/10.3389/fneur.2018.00144.CrossRefGoogle Scholar
  5. Aytekin, M., Victor, J. D., & Rucci, M. (2014). The visual input to the retina during natural head-free fixation. The Journal of Neuroscience, 34(38), 12701–12715.CrossRefPubMedPubMedCentralGoogle Scholar
  6. Bair, W., & O’Keefe, L. P. (1998). The influence of fixational eye movements on the response of neurons in area MT of the macaque. Visual Neuroscience, 15, 779–786.Google Scholar
  7. Barlow, H. B. (1952). Eye movements during fixation. Journal of Physiology, 116, 290–306.CrossRefPubMedGoogle Scholar
  8. Beer, A. L. et al. (2008). A motion illusion reveals mechanisms of perceptual stabilization. PLoS ONE, 3, e2741.CrossRefPubMedPubMedCentralGoogle Scholar
  9. Benedetto, S., Pedrotti, M., & Bridgeman, B. (2011). Microsaccades and exploratory saccades in a naturalistic environment. Journal of Eye Movement Research, 4(2), 1–10.Google Scholar
  10. Bengi, H., & Thomas, J. (1968). Three electronic methods for recording ocular tremor. Medical and Biological Engineering, 6(2), 171–179.CrossRefPubMedGoogle Scholar
  11. Betta, E., & Turatto, M. (2006). Are you ready? I can tell by looking at your microsaccades. NeuroReport, 17(10), 1001–1004.CrossRefPubMedGoogle Scholar
  12. Betta, E. et al. (2007). Microsaccadic response during inhibition of return in a target-target paradigm. Vision Research, 47, 428–436.CrossRefPubMedGoogle Scholar
  13. Billino, J., Hamburger, K., & Gegenfurtner, K. R. (2009). Age effects on the perception of motion illusions. Perception, 38(4), 508–521.CrossRefPubMedGoogle Scholar
  14. Bosman, C. A. et al. (2009). A microsaccadic rhythm modulates gammaband synchronization and behavior. Journal of Neuroscience, 29, 9471–9480.CrossRefPubMedGoogle Scholar
  15. Boyce, P. R. (1967). Monocular fixation in human eye movement. Proceedings of the Royal Society of London. B, 167, 293–315.Google Scholar
  16. Boyle, G., Coakley, D., & Malone, J. F. (2001). Interferometry for ocular microtremor measurement. Applied Optics, 40(1), 167–175.CrossRefPubMedGoogle Scholar
  17. Bridgeman, B., & Palca, J. (1980). The role of microsaccades in high acuity observational tasks. Vision Research, 20(9), 813–817.CrossRefPubMedGoogle Scholar
  18. Brien, D. C., Corneil, J. H., Fecteau, J. H., Bell, A. H., & Munoz, D. P. (2009). The behavioural and neurophysiological modulation of microsaccades in monkeys. Journal of Eye Movement Research, 3, 1–12.Google Scholar
  19. Carpenter, R. H. S. (1988). Movements of the eyes (2nd ed.). London: Pion Ltd.Google Scholar
  20. Cherici, C., Kuang, X., Poletti, M., & Rucci, M. (2012). Precision of sustained fixation in trained and untrained observers. Journal of Vision, 12(6).Google Scholar
  21. Collewijn, H., & Kowler, E. (2008). The significance of microsaccades for vision and oculomotor control. Journal of Vision, 8(14).  https://doi.org/10.1167/8.14.20.CrossRefPubMedPubMedCentralGoogle Scholar
  22. Cornsweet, T. N. (1956). Determination of the stimuli for involuntary drifts and saccadic eye movements. The Journal of the Optical Society of America, 46(11), 987–993.CrossRefPubMedGoogle Scholar
  23. Costela, F. M., McCamy, M. B., Macknik, S. L., Otero-Millan, J., & Martinez-Conde, S. (2013a). Microsaccades restore the visibility of minute foveal targets. PeerJ, 1, e119.  https://doi.org/10.7717/peerj.119.CrossRefPubMedPubMedCentralGoogle Scholar
  24. Costela, F. M., Otero-Millan, J., McCamy, M. B., Macknik, S. L., Troncoso, X. G., Jazi, A. N., & Martinez-Conde, S. (2014). Fixational eye movement correction of blink-induced gaze position errors. PLoS ONE, 9(10), e110889.  https://doi.org/10.1371/journal.pone.0110889.CrossRefPubMedPubMedCentralGoogle Scholar
  25. Costela, F. M., Otero-Millan, J., McCamy, M. B., Macknik, S. L., Troncoso, X., & Martinez-Conde, S. (2013). Microsaccades correct fixation errors due to blinks. Journal of Vision, 13(9), 1335–1335.Google Scholar
  26. Cui, J. et al. (2009). Visibility states modulate microsaccade rate and direction. Vision Research, 49, 228–236.CrossRefPubMedGoogle Scholar
  27. Di Stasi, L. L., Cabestrero, R., McCamy, M. B., Ríos, F., Catena, A., Quirós, P., & Martinez-Conde, S. (2014a). Intersaccadic drift velocity is sensitive to short-term hypobaric hypoxia. The European Journal of Neuroscience, 39(8), 1384–1390.  https://doi.org/10.1111/ejn.12482.CrossRefPubMedGoogle Scholar
  28. Di Stasi, L. L., Catena, A., Cañas, J. J., Macknik, S. L., & Martinez-Conde, S. (2013a). Saccadic velocity as an arousal index in naturalistic tasks. Neuroscience and Biobehavioral Reviews, 37(5), 968–975.  https://doi.org/10.1016/j.neubiorev.2013.03.011.CrossRefPubMedGoogle Scholar
  29. Di Stasi, L. L., McCamy, M. B., Catena, A., Macknik, S. L., Cañas, J. J., & Martinez-Conde, S. (2013b). Microsaccade and drift dynamics reflect mental fatigue. The European Journal of Neuroscience, 38(3), 2389–2398.  https://doi.org/10.1111/ejn.12248.CrossRefPubMedGoogle Scholar
  30. Di Stasi, L. L., McCamy, M. B., Macknik, S. L., Mankin, J. A., Hooft, N., Catena, A., & Martinez-Conde, S. (2014b). Saccadic eye movement metrics reflect surgical residents’ fatigue. Annals of Surgery, 259(4), 824–829.CrossRefPubMedGoogle Scholar
  31. Di Stasi, L. L., McCamy, M. B., Pannasch, S., Renner, R., Catena, A., Cañas, J. J., & Martinez-Conde, S. (2015). Effects of driving time on microsaccadic dynamics. Experimental Brain Research, 233(2), 599–605.CrossRefPubMedGoogle Scholar
  32. Dimigen, O., Valsecchi, M., Sommer, W., & Kliegl, R. (2009). Human microsaccade-related visual brain responses. Journal of Neuroscience, 29(39), 12321–12331.CrossRefPubMedGoogle Scholar
  33. Ditchburn, R. W., & Foley-Fisher, J. A. (1967). Assembled data in eye movements. Optica Acta (Lond), 14(2), 113–118.CrossRefGoogle Scholar
  34. Ditchburn, R. W., & Ginsborg, B. L. (1952). Vision with a stabilized retinal image. Nature, 170, 36–37.CrossRefPubMedGoogle Scholar
  35. Ditchburn, R. W., & Ginsborg, B. L. (1953). Involuntary eye movements during fixation. Journal of Physiology, 119(1), 1–17.CrossRefPubMedGoogle Scholar
  36. Donner, K., & Hemila, S. (2007). Modelling the effect of microsaccades on retinal responses to stationary contrast patterns. Vision Research, 47(9), 1166–1177.CrossRefPubMedGoogle Scholar
  37. Eizenman, M., Hallett, P. E., & Frecker, R. C. (1985). Power spectra for ocular drift and tremor. Vision Research, 25(11), 1635–1640.CrossRefPubMedGoogle Scholar
  38. Engbert, R. (2012). Computational modeling of collicular integration of perceptual responses and attention in microsaccades. Journal of Neuroscience, 32(23), 8035–8039.  https://doi.org/10.1523/JNEUROSCI.0808-12.2012.CrossRefPubMedGoogle Scholar
  39. Engbert, R., & Kliegl, R. (2003a). Microsaccades uncover the orientation of covert attention. Vision Research, 43(9), 1035–1045.CrossRefPubMedGoogle Scholar
  40. Engbert, R., & Kliegl, R. (2003b). The mind’s eyes: Cognitive and applied aspects of eye movements. In: J. Hyona, R. Radach & H. Deubel (Eds.) (pp. 103–117), Oxford: Elsevier.Google Scholar
  41. Engbert, R., & Kliegl, R. (2004). Microsaccades keep the eyes’ balance during fixation. Psychological Science, 15(6), 431–436.CrossRefPubMedGoogle Scholar
  42. Engbert, R., & Mergenthaler, K. (2006). Microsaccades are triggered by low retinal image slip. Proceedings of the National Academy of Sciences of the United States of America, 103, 7192–7197.Google Scholar
  43. Engbert, R., Mergenthaler, K., Sinn, P., & Pikovsky, A. (2011). An integrated model of fixational eye movements and microsaccades. Proceedings of the National Academy of Sciences of the United States of America, 108(39), E765–770.Google Scholar
  44. Falkenberg, H. K., Rubin, G. S., & Bex, P. J. (2007). Acuity, crowding, reading and fixation stability. Vision Research, 47(1), 126–135.CrossRefPubMedGoogle Scholar
  45. Findlay, J., & Gilchrist, I. (2003). Active vision: The psychology of seeing and looking. Oxford: Oxford University Press.CrossRefGoogle Scholar
  46. Fiorentini, A., & Ercoles, A. M. (1966). Involuntary eye movements during attempted monocular fixation. Atti della Fondazione Giorgio Ronchi, 21, 199–217.Google Scholar
  47. Galfano, G. et al. (2004). Inhibition of return in microsaccades. Experimental Brain Research, 159, 400–404.CrossRefPubMedGoogle Scholar
  48. Gandhi, N. J., & Keller, E. L. (1999). Activity of the brain stem omnipause neurons during saccades perturbed by stimulation of the primate superior colliculus. Journal of Neurophysiology, 82(6), 3254–3267.CrossRefPubMedGoogle Scholar
  49. Goffart, L. et al. (2006). Influence of background illumination on fixation and visually guided saccades in the rhesus monkey. Vision Research, 46, 149–162.CrossRefPubMedGoogle Scholar
  50. Gowen, E., Abadi, R. V., Poliakoff, E., Hansen, P. C., & Miall, R. C. (2007). Modulation of saccadic intrusions by exogenous and endogenous attention. Brain Research, 1141, 154–167.  https://doi.org/10.1016/j.brainres.2007.01.047.CrossRefPubMedPubMedCentralGoogle Scholar
  51. Greschner, M., Bongard, M., Rujan, P., & Ammermuller, J. (2002). Retinal ganglion cell synchronization by fixational eye movements improves feature stimation. Nature Neuroscience, 5(4), 341–347.CrossRefPubMedGoogle Scholar
  52. Guitton, D., & Munoz, D. P. (1991). Control of orienting gaze shifts by the tectoreticulospinal system in the head-free cat. I. Identification, localization, and effects of behavior on sensory responses. Journal of Neurophysiology, 66(5), 1605–1623.Google Scholar
  53. Hafed, Z. M., & Clark, J. J. (2002). Microsaccades as an overt measure of covert attention shifts. Vision Research, 42(22), 2533–2545.CrossRefPubMedGoogle Scholar
  54. Hafed, Z. M., Goffart, L., & Krauzlis, R. (2009). A neural mechanism for microsaccade generation in the primate superior colliculus. Science, 323(5916), 940–943.CrossRefPubMedPubMedCentralGoogle Scholar
  55. Herrington, T. M. et al. (2009). The effect of microsaccades on the correlation between neural activity and behavior in middle temporal, ventral intraparietal, and lateral intraparietal areas. Journal of Neuroscience, 29, 5793–5805.CrossRefPubMedGoogle Scholar
  56. Horwitz, G. D., & Albright, T. D. (2003). Short-latency fixational saccades induced by luminance increments. Journal of Neurophysiology, 90, 1333–1339.Google Scholar
  57. Horowitz, T. S., Fine, E. M., Fencsik, D. E., Yurgenson, S., & Wolfe, J. M. (2007). Fixational eye movements are not an index of covert attention. Psychological Science, 18(4), 356–363.CrossRefPubMedGoogle Scholar
  58. Hubel, D. H. (1988). Eye, brain, and vision (Vol. 22). New York: Scientific American Library.Google Scholar
  59. Jurin. (1738). Essay on distinct and indistintc vision. Optics.Google Scholar
  60. Kagan, I. et al. (2008). Saccades and drifts differentially modulate neuronal activity in V1: Effects of retinal image motion, position, and extraretinal influences. Journal of Vision, 8(14), 19, 11–25.CrossRefPubMedGoogle Scholar
  61. Kingstone, A., Fendrich, R., Wessinger, C. M., & ReuterLorenz, P. A. (1995). Are microsaccades responsible for the gap effect? Perception & Psychophysics, 57, 796–801.Google Scholar
  62. Kitaoka, A. (2003). Akiyoshi’s illusion pages. Retrieved from http://www.ritsumei.ac.jp/~akitaoka/index-e.html.
  63. Kliegl, R. et al. (2009). Microsaccadic modulation of response times in spatial attention tasks. Psychological Research, 73, 136–146.CrossRefPubMedGoogle Scholar
  64. Ko, H.-K., Poletti, M., & Rucci, M. (2010). Microsaccades precisely relocate gaze in a high visual acuity task. Nature Neuroscience, 13(12), 1549–1553.  https://doi.org/10.1038/nn.2663.CrossRefPubMedPubMedCentralGoogle Scholar
  65. Ko, H.-K., Snodderly, D. M., & Poletti, M. (2016). Eye movements between saccades: Measuring ocular drift and tremor. Vision Research, 122, 93–104.CrossRefPubMedPubMedCentralGoogle Scholar
  66. Kowler, E., & Steinman, R. M. (1980). Small saccades serve no useful purpose: Reply to a letter by R. W. Ditchburn. Vision Research, 20(3), 273–276.CrossRefPubMedGoogle Scholar
  67. Krauskopf, J. (1967). Heterochromatic stabilized images: A classroom demonstration. American Journal of Psychology, 80(4), 634–637.CrossRefPubMedGoogle Scholar
  68. Krauskopf, J. et al. (1960). Analysis of eye movements during monocular and binocular fixation. Journal of the Optical Society of America, 50, 572–578.CrossRefPubMedGoogle Scholar
  69. Kuang, X., Poletti, M., Victor, J. D., & Rucci, M. (2012). Temporal encoding of spatial information during active visual fixation. Current Biology, 22(6), 510–514.CrossRefPubMedPubMedCentralGoogle Scholar
  70. Laubrock, J., Engbert, R., & Kliegl, R. (2005). Microsaccade dynamics during covert attention. Vision Research, 45(6), 721–730.  https://doi.org/10.1016/j.visres.2004.09.029.CrossRefPubMedGoogle Scholar
  71. Laubrock, J., Engbert, R., & Kliegl, R. (2008). Fixational eye movements predict the perceived direction of ambiguous apparent motion. Journal of Vision, 8(14):13, 1–17.Google Scholar
  72. Laubrock, J., Engbert, R., Rolfs, M., & Kliegl, R. (2007). Microsaccades are an index of covert attention: Commentary on Horowitz, Fine, Fencsik, Yurgenson, and Wolfe (2007). Psychological Science, 18(4), 364–366; discussion 367–368.Google Scholar
  73. Laubrock, J., Kliegl, R., Rolfs, M., & Engbert, R. (2010). When do microsaccades follow spatial attention? Attention, Perception, & Psychophysics, 72(3), 683–694.  https://doi.org/10.3758/APP.72.3.683.CrossRefGoogle Scholar
  74. Leigh, R. J., & Zee, D. S. (2015). The neurology of eye movements (5th ed.). Oxford: Oxford University Press.Google Scholar
  75. Leopold, D. A., & Logothetis, N. K. (1998). Microsaccades differentially modulate neural activity in the striate and extrastriate visual cortex. Experimental Brain Research, 123, 341–345.Google Scholar
  76. Liang, J. R., Moshel, S., Zivotofsky, A. Z., Caspi, A., Engbert, R., Kliegl, R. et al. (2005). Scaling of horizontal and vertical fixational eye movements. Physical Review E, 71, 031909.Google Scholar
  77. Lord, M. P. (1951). Measurement of binocular eye movements of subjects in the sitting position. British Journal of Ophthalmology, 35, 21–30.CrossRefPubMedGoogle Scholar
  78. Lord, M. P., & Wright, W. D. (1948). Eye movements during monocular fixation. Nature, 162, 25–26.Google Scholar
  79. Macknik, S. L., & Martinez-Conde, S. (2016). The age of illusion. Scientific American Mind, 27(1), 18–19.CrossRefGoogle Scholar
  80. Malinov, I. V., Epelboim, J., Herst, A. N., & Steinman, R. M. (2000). Characteristics of saccades and vergence in two types of sequential looking tasks. Vision Research, 40, 2083–2090.Google Scholar
  81. Martinez-Conde, S. (2006). Fixational eye movements in normal and pathological vision. Progress in Brain Research, 154, 151–176.  https://doi.org/10.1016/s0079-6123(06)54008-7.CrossRefPubMedGoogle Scholar
  82. Martinez-Conde, S., & Alexander, R. G. (2019). A gaze bias in the mind’s eye. Nature Human Behaviour, 3(5), 424–425. https://doi.org/10.1038/s41562-019-0546-1.CrossRefPubMedGoogle Scholar
  83. Martinez-Conde, S., & Macknik, S. L. (2007). Windows on the mind. Scientific American, 297(2), 56–63.Google Scholar
  84. Martinez-Conde, S., & Macknik, S. L. (2015). From exploration to fixation: An integrative view of Yarbus’s vision. Perception, 44(8–9), 884–899.  https://doi.org/10.1177/0301006615594963.CrossRefPubMedGoogle Scholar
  85. Martinez-Conde, S., Macknik, S. L., & Hubel, D. H. (2000). Microsaccadic eye movements and firing of single cells in the striate cortex of macaque monkeys [published erratum appears in Nature Neuroscience 2000 Apr; 3(4):409]. Nature Neuroscience, 3(3), 251–258.  https://doi.org/10.1038/72961.CrossRefPubMedGoogle Scholar
  86. Martinez-Conde, S., Macknik, S. L., & Hubel, D. H. (2002). The function of bursts of spikes during visual fixation in the awake primate lateral geniculate nucleus and primary visual cortex. Proceedings of the National Academy of Sciences of the United States of America, 99(21), 13920–13925.  https://doi.org/10.1073/pnas.212500599.CrossRefPubMedPubMedCentralGoogle Scholar
  87. Martinez-Conde, S., Macknik, S. L., & Hubel, D. H. (2004). The role of fixational eye movements in visual perception. Nature Reviews Neuroscience, 5(3), 229–240.  https://doi.org/10.1038/nrn1348.CrossRefPubMedGoogle Scholar
  88. Martinez-Conde, S., Macknik, S. L., Troncoso, X. G., & Dyar, T. A. (2006). Microsaccades counteract visual fading during fixation. Neuron, 49(2), 297–305.  https://doi.org/10.1016/j.neuron.2005.11.033. S0896-6273(05)01056-1 [pii].CrossRefPubMedGoogle Scholar
  89. Martinez-Conde, S., Macknik, S. L., Troncoso, X. G., & Hubel, D. H. (2009). Microsaccades: A neurophysiological analysis. Trends in Neurosciences, 32(9), 463–475.  https://doi.org/10.1016/j.tins.2009.05.006.CrossRefPubMedGoogle Scholar
  90. Martinez-Conde, S., Otero-Millan, J., & Macknik, S. L. (2013). The impact of microsaccades on vision: Towards a unified theory of saccadic function. Nature Reviews Neuroscience, 14(2), 83–96.  https://doi.org/10.1038/nrn3405.CrossRefPubMedGoogle Scholar
  91. McCamy, M. B., Collins, N., Otero-Millan, J., Al-Kalbani, M., Macknik, S. L., Coakley, D., & Wolf. T. R. (2013a). Simultaneous recordings of ocular microtremor and microsaccades with a piezoelectric sensor and a video-oculography system. PeerJ, 1, e14.  https://doi.org/10.7717/peerj.14.CrossRefPubMedPubMedCentralGoogle Scholar
  92. McCamy, M. B., Macknik, S. L., & Martinez-Conde, S. (2013b). Natural eye movements and vision. In J. S. Werner & L. M. Chalupa (Eds.), The new visual neurosciences. Cambridge, MA: The MIT Press.Google Scholar
  93. McCamy, M. B., Najafian Jazi, A., Otero-Millan, J., Macknik, S. L., & Martinez-Conde, S. (2013c). The effects of fixation target size and luminance on microsaccades and square-wave jerks. PeerJ, 1, e9.  https://doi.org/10.7717/peerj.9.CrossRefPubMedPubMedCentralGoogle Scholar
  94. McCamy, M. B., Macknik, S. L., & Martinez-Conde, S. (2014a). Different fixational eye movements mediate the prevention and the reversal of visual fading. The Journal of Physiology, 592(19), 4381–4394.  https://doi.org/10.1113/jphysiol.2014.279059.CrossRefPubMedPubMedCentralGoogle Scholar
  95. McCamy, M. B., Otero-Millan, J., Di Stasi, L. L., Macknik, S. L., & Martinez-Conde, S. (2014b). Highly informative natural scene regions increase microsaccade production during visual scanning. The Journal of Neuroscience, 34(8), 2956–2966.  https://doi.org/10.1523/jneurosci.4448-13.2014.CrossRefPubMedGoogle Scholar
  96. McCamy, M. B., Otero-Millan, J., Leigh, R. J., King, S. A., Schneider, R. M., Macknik, S. L., & Martinez-Conde, S. (2015). Simultaneous recordings of human microsaccades and drifts with a contemporary video eye tracker and the search coil technique. PLoS ONE, 10(6), e0128428.  https://doi.org/10.1371/journal.pone.0128428.CrossRefPubMedPubMedCentralGoogle Scholar
  97. McCamy, M. B., Otero-Millan, J., Macknik, S. L., Yang, Y., Troncoso, X. G., Baer, S. M., & Martinez-Conde, S. (2012). Microsaccadic efficacy and contribution to foveal and peripheral vision. Journal of Neuroscience, 32(27), 9194–9204.  https://doi.org/10.1523/JNEUROSCI.0515-12.2012.CrossRefPubMedGoogle Scholar
  98. Meirovithz, E., Ayzenshtat, I., Werner-Reiss, U., Shamir, I., & Slovin, H. (2012). Spatiotemporal effects of microsaccades on population activity in the visual cortex of monkeys during fixation. Cerebral Cortex, 22(2), 294–307.CrossRefPubMedGoogle Scholar
  99. Mergenthaler, K., & Engbert, R. (2007). Modeling the control of fixational eye movements with neurophysiological delays. Physical Review Letters, 98, 138104.Google Scholar
  100. Mergenthaler, K., & Engbert, R. (2010). Microsaccades are different from saccades in scene perception. Experimental Brain Research, 203(4), 753–757.CrossRefPubMedGoogle Scholar
  101. Meyberg, S., Werkle-Bergner, M., Sommer, W., & Dimigen, O. (2015). Microsaccade-related brain potentials signal the focus of visuospatial attention. Neuroimage, 104, 79–88.CrossRefPubMedGoogle Scholar
  102. Moller, F., Laursen, M. L., Tygesen, J., & Sjolie, A. K. (2002). Binocular quantification and characterization of microsaccades. Graefes Archive for Clinical and Experimental Ophthalmology, 240(9), 765–770.  https://doi.org/10.1007/s00417-002-0519-2.CrossRefGoogle Scholar
  103. Moschovakis, A., Scudder, C., & Highstein, S. (1996). The microscopic anatomy and physiology of the mammalian saccadic system. Progress in Neurobiology, 50(2), 133–254.CrossRefPubMedGoogle Scholar
  104. Moshel, S. et al. (2008). Persistence and phase synchronization properties of fixational eye movements. European Physical Journal Special Topics, 161, 207–223.CrossRefGoogle Scholar
  105. Munoz, D. P. (2002). Commentary: Saccadic eye movements: Overview of neural circuitry. Progress in Brain Research, 140, 89–96.CrossRefPubMedGoogle Scholar
  106. Munoz, D. P., & Wurtz, R. H. (1995). Saccade-related activity in monkey superior colliculus. I. Characteristics of burst and buildup cells. Journal of Neurophysiology, 73(6), 2313–2333.Google Scholar
  107. Murakami, I. (2006). Fixational eye movements and motion perception. Progress in Brain Research, 154, 193–209.CrossRefPubMedGoogle Scholar
  108. Murakami, I., & Cavanagh, P. (1998). A jitter after-effect reveals motion-based stabilization of vision. Nature, 395, 798–801.CrossRefPubMedGoogle Scholar
  109. Murakami, I., & Cavanagh, P. (2001). Visual jitter: Evidence for visual-motion-based compensation of retinal slip due to small eye movements. Vision Research, 41(2), 173–186.CrossRefPubMedGoogle Scholar
  110. Murakami, I., Kitaoka, A., & Ashida, H. (2006). A positive correlation between fixation instability and the strength of illusory motion in a static display. Vision Research, 46(15), 2421–2431.CrossRefPubMedGoogle Scholar
  111. Müri, R., Nyffeler, T., & Cazzoli, D. (2019). Neurology. In C. Klein & U. Ettinger (Eds.), Eye movement research: An introduction to its scientific foundations and applications. Berlin: Springer Publishers.Google Scholar
  112. Nachmias, J. (1959). Two-dimensional motion of the retinal image during monocular fixation. Journal of the Optical Society of America, 49, 901–908.CrossRefPubMedGoogle Scholar
  113. Nachmias, J. (1961). Determiners of the drift of the eye during monocular fixation. Journal of the Optical Society of America, 51, 761–766.CrossRefPubMedGoogle Scholar
  114. Nyström, M., Hansen, D. W., Andersson, R., & Hooge, I. (2014). Why have microsaccades become larger? Investigating eye deformations and detection algorithms. Vision Research.Google Scholar
  115. Optican, L. M. (1995). A field theory of saccade generation: Temporal-to-spatial transform in the superior colliculus. Vision Research, 35(23), 3313–3320.CrossRefPubMedGoogle Scholar
  116. Otero-Millan, J., Macknik, S. L., Langston, R. E., & Martinez-Conde, S. (2013a). An oculomotor continuum from exploration to fixation. Proceedings of the National Academy of Sciences of the United States of America, 110(15), 6175–6180.  https://doi.org/10.1073/pnas.1222715110.CrossRefPubMedPubMedCentralGoogle Scholar
  117. Otero-Millan, J., Troncoso, X. G., Macknik, S. L., Serrano-Pedraza, I., & Martinez-Conde, S. (2008). Saccades and microsaccades during visual fixation, exploration, and search: Foundations for a common saccadic generator. Journal of Vision, 8(14), 1–18, 21.  https://doi.org/10.1167/8.14.21/8/14/21.
  118. Otero-Millan, J., Macknik, S. L., & Martinez-Conde, S. (2012). Microsaccades and blinks trigger illusory rotation in the “rotating snakes” illusion. Journal of Neuroscience, 32(17), 6043–6051.  https://doi.org/10.1523/JNEUROSCI.5823-11.2012.CrossRefPubMedGoogle Scholar
  119. Otero-Millan, J., Macknik, S. L., Serra, A., Leigh, R. J., & Martinez-Conde, S. (2011). Triggering mechanisms in microsaccade and saccade generation: A novel proposal. Annals of the New York Academy of Sciences, 1233(1), 107–116.  https://doi.org/10.1111/j.1749-6632.2011.06177.x.CrossRefPubMedGoogle Scholar
  120. Otero-Millan, J., Schneider, R., Leigh, R. J., Macknik, S. L., & Martinez-Conde, S. (2013b). Saccades during Attempted Fixation in Parkinsonian Disorders and Recessive Ataxia: From microsaccades to square-wave jerks. PLoS ONE, 8(3), e58535.  https://doi.org/10.1371/journal.pone.0058535.CrossRefPubMedPubMedCentralGoogle Scholar
  121. Pinnock, R. A., McGivern, R. C., Forbes, R., & Gibson, J. M. (2010). An exploration of ocular fixation in Parkinson’s disease, multiple system atrophy and progressive supranuclear palsy. Journal of Neurology.Google Scholar
  122. Poletti, M., Listorti, C., & Rucci, M. (2013). Microscopic eye movements compensate for nonhomogeneous vision within the fovea. Current Biology, 23(17), 1691–1695.CrossRefPubMedGoogle Scholar
  123. Poletti, M., & Rucci, M. (2010). Eye movements under various conditions of image fading. Journal of Vision, 10(3), 6 1–18.Google Scholar
  124. Pritchard, R. M. (1961). Stabilized images on the retina. Scientific American, 204, 72–78.CrossRefPubMedGoogle Scholar
  125. Ratliff, F., & Riggs, L. A. (1950). Involuntary motions of the eye during monocular fixation. Journal of Experimental Psychology, 40, 687–701.Google Scholar
  126. Riggs, L. A., & Ratliff, F. (1951). Visual acuity and the normal tremor of the eyes. Science, 114(2949), 17–18.CrossRefPubMedGoogle Scholar
  127. Riggs, L. A., & Ratliff, F. (1952). The effects of counteracting the normal movements of the eye. Journal of the Optical Society of America, 42, 872–873.Google Scholar
  128. Riggs, L. A., Armington, J. C., & Ratliff, F. (1954). Motions of the retinal image during fixation. Journal of the Optical Society of America, 44, 315–321.Google Scholar
  129. Robinson, D. A. (1973). Models of the saccadic eye movement control system. Kybernetik, 14(2), 71–83.CrossRefPubMedGoogle Scholar
  130. Rolfs, M. (2009). Microsaccades: Small steps on a long way. Vision Research, 49(20), 2415–2441.  https://doi.org/10.1016/j.visres.2009.08.010. S0042-6989(09)00369-1 [pii].CrossRefPubMedGoogle Scholar
  131. Rolfs, M., Engbert, R., & Kliegl, R. (2004). Microsaccade orientation supports attentional enhancement opposite a peripheral cue: Commentary on Tse, Sheinberg, and Logothetis (2003). Psychological Science, 15(10), 705–707; author reply 708–710.  https://doi.org/10.1111/j.0956-7976.2004.00744.x.CrossRefPubMedGoogle Scholar
  132. Rolfs, M. et al. (2005). Crossmodal coupling of oculomotor control and spatial attention in vision and audition. Experimental Brain Research, 166, 427–439.CrossRefPubMedGoogle Scholar
  133. Rolfs, M., Kliegl, R., & Engbert, R. (2008). Toward a model of microsaccade generation: The case of microsaccadic inhibition. Journal of Vision, 8(11), 5, 1–23.  https://doi.org/10.1167/8.11.5.CrossRefPubMedGoogle Scholar
  134. Rolfs, M., Laubrock, J., & Kliegl, R. (2006). Shortening and prolongation of saccade latencies following microsaccades. Experimental Brain Research, 169(3), 369–376.  https://doi.org/10.1007/s00221-005-0148-1.CrossRefPubMedGoogle Scholar
  135. Rolfs, M., Laubrock, J., & Kliegl, R. (2008). Microsaccade-induced prolongation of saccadic latencies depends on microsaccade amplitude. Journal of Eye Movement Research, 1(3), 1, 1–8.Google Scholar
  136. Rucci, M., Iovin, R., Poletti, M., & Santini, F. (2007). Miniature eye movements enhance fine spatial detail. Nature, 447(7146), 851–854.  https://doi.org/10.1038/nature05866.CrossRefPubMedGoogle Scholar
  137. Rucci, M., & Poletti, M. (2015). Control and functions of fixational eye movements. Annual Review of Vision Science, 1, 499–518.CrossRefPubMedPubMedCentralGoogle Scholar
  138. Rucci, M., & Victor, J. D. (2015). The unsteady eye: An information-processing stage, not a bug. Trends in Neurosciences, 38(4), 195–206.CrossRefPubMedPubMedCentralGoogle Scholar
  139. Ryle, J. P., Al-Kalbani, M., Collins, N., Gopinathan, U., Boyle, G., Coakley, D., & Sheridan, J. T. (2009). Compact portable ocular microtremor sensor: Design, development and calibration. Journal of Biomedical Optics, 14(1), 014021-014021-014012.Google Scholar
  140. Sabrin, H. W., & Kertesz, A. E. (1980). Microsaccadic eye movements and binocular rivalry. Perception & Psychophysics, 28, 150–154.Google Scholar
  141. Sansbury, R. V., Skavenski, A. A., Haddad, G. M., & Steinman, R. M. (1973). Normal fixation of eccentric targets. Journal of the Opical Society of America, 63, 612–614.Google Scholar
  142. Schiller, P. H. (1984). The superior colliculus and visual function. In D.-S. I. (Ed.), Handbook of physiology—The nervous system III. Sensory processes part I. Bethesda MD: American Physiological Society.Google Scholar
  143. Schulz, E. (1984). Binocular micromovements in normal persons. Graefe’s Archive for Clinical and Experimental Ophthalmology, 222, 95–100.CrossRefPubMedGoogle Scholar
  144. Schiller, P. H., & Stryker, M. (1972). Single-unit recording and stimulation in superior colliculus of the alert rhesus monkey. Journal of Neurophysiology, 35, 915–924.CrossRefPubMedGoogle Scholar
  145. Scudder, C. A., Kaneko, C. R., & Fuchs, A. F. (2002). The brainstem burst generator for saccadic eye movements. Experimental Brain Research, 142(4), 439–462.CrossRefPubMedGoogle Scholar
  146. Simons, D., Lleras, A., Martinez-Conde, S., Slichter, D., Caddigan, E., & Nevarez, G. (2006). Induced visual fading of complex images. Journal of Vision, 6, 1093–1101.CrossRefPubMedGoogle Scholar
  147. Skavenski, A. A., Robinson, D. A., Steinman, R. M., & Timberlake, G. T. (1975). Miniature eye movements of fixation in rhesus monkey. Vision Research, 15(11), 1269–1273.CrossRefPubMedGoogle Scholar
  148. Snodderly, D. M., Kagan, I., & Gur, M. (2001). Selective activation of visual cortex neurons by fixational eye movements: Implications for neural coding. Visual Neuroscience, 18, 259–277.Google Scholar
  149. Sparks, D. L. (2002). The brainstem control of saccadic eye movements. Nature Reviews Neuroscience, 3(12), 952–964.CrossRefPubMedGoogle Scholar
  150. Spauschus, A., Marsden, J., Halliday, D. M., Rosenberg, J. R., & Brown, P. (1999). The origin of ocular microtremor in man. Experimental Brain Research, 126(4), 556–562.CrossRefPubMedGoogle Scholar
  151. Srebro, R. (1983). Fixation of normal and amblyopic eyes. Archives of Ophthalmology, 101, 214–217.CrossRefPubMedGoogle Scholar
  152. Stanford, T. R., Freedman, E. G., & Sparks, D. L. (1996). Site and parameters of microstimulation: Evidence for independent effects on the properties of saccades evoked from the primate superior colliculus. Journal of Neurophysiology, 76(5), 3360–3381.CrossRefPubMedGoogle Scholar
  153. Steinman, R. M. (1965). Effect of target size, luminance, and color on monocular fixation. Journal of the Optical Society of America, 55, 1158–1165.CrossRefGoogle Scholar
  154. Steinman, R. M., Cunitz, R. J., Timberlake, G. T., & Herman, M. (1967). Voluntary control of microsaccades during maintained monocular fixation. Science, 155(769), 1577–1579.CrossRefPubMedGoogle Scholar
  155. Steinman, R. M. et al. (1973). Miniature eye movement. Science, 181, 810–819.CrossRefPubMedGoogle Scholar
  156. Stevens, J. K., Emerson, R. C., Gerstein, G. L., Kallos, T., Neufeld, G. R., Nichols, C. W., & Rosenquis, A. C. (1976). Paralysis of the awake human: Visual perceptions. Vision Research, 16(1), 93–98.CrossRefPubMedGoogle Scholar
  157. Thaler, L., Schutz, A. C., Goodale, M. A., & Gegenfurtner, K. R. (2013). What is the best fixation target? The effect of target shape on stability of fixational eye movements. Vision Research, 76, 31–42.  https://doi.org/10.1016/j.visres.2012.10.012. S0042-6989(12)00338-0 [pii].CrossRefPubMedGoogle Scholar
  158. Troncoso, X. G., Macknik, S. L., & Martinez-Conde, S. (2008). Microsaccades counteract perceptual filling-in. Journal of Vision, 8(14), 15, 11–19.  https://doi.org/10.1167/8.14.15.CrossRefPubMedGoogle Scholar
  159. Troncoso, X. G., Macknik, S. L., Otero-Millan, J., & Martinez-Conde, S. (2008). Microsaccades drive illusory motion in the Enigma illusion. Proceedings of the National Academy of Sciences, 105(41), 16033–16038.  https://doi.org/10.1073/pnas.0709389105. 0709389105 [pii].CrossRefGoogle Scholar
  160. Tse, P. U., Baumgartner, F. J., & Greenlee, M. W. (2010). Event-related functional MRI of cortical activity evoked by microsaccades, small visually-guided saccades, and eyeblinks in human visual cortex. Neuroimage, 49(1), 805–816.CrossRefPubMedGoogle Scholar
  161. Turatto, M., Valsecchi, M., Tame, L., & Betta, E. (2007). Microsaccades distinguish between global and local visual processing. NeuroReport, 18(10), 1015–1018.CrossRefPubMedGoogle Scholar
  162. Valsecchi, M., & Turatto, M. (2007). Microsaccadic response to visual events that are invisible to the superior colliculus. Behavioral Neuroscience, 121, 786–793.Google Scholar
  163. Valsecchi, M., & Turatto, M. (2009). Microsaccadic responses in a bimodal oddball task. Psychological Research, 73, 23–33.Google Scholar
  164. van Dam, L. C., & van Ee, R. (2005). The role of (micro)saccades and blinks in perceptual bi-stability from slant rivalry. Vision Research, 45, 2417–2435.Google Scholar
  165. Van der Geest, J., & Frens, M. (2002). Recording eye movements with video-oculography and scleral search coils: A direct comparison of two methods. Journal of Neuroscience Methods, 114(2), 185–195.CrossRefPubMedGoogle Scholar
  166. Van Ede, F., Chekroud, S. R. & Nobre, A. C. (2019). Human gaze tracks attentional focusing in memorized visual space. Nature Human Behaviour. https://doi.org/10.1038/s41562-019-0549-y.CrossRefPubMedPubMedCentralGoogle Scholar
  167. Verheijen, F. (1961). A simple after image method demonstrating the involuntary multidirectional eye movements during fixation. Journal of Modern Optics, 8(4), 309–312.Google Scholar
  168. West, D. C., & Boyce, P. R. (1968). The effect of flicker on eye movement. Vision Research, 8, 171–192.Google Scholar
  169. Winterson, B. J., & Collewijn, H. (1976). Microsaccades during finely guided visuomotor tasks. Vision Research, 16(12), 1387–1390.CrossRefPubMedGoogle Scholar
  170. Yarbus, A. L. (1957). The perception of an image fixed with respect to the retina. Biophysics, 2, 683–690.Google Scholar
  171. Yarbus, A. L. (1967). Eye Movements and vision (B. Haigh, Trans.). New York: Plenum Press.Google Scholar
  172. Yuval-Greenberg, S. et al. (2008). Transient induced gamma-band response in EEG as a manifestation of miniature saccades. Neuron, 58, 429–441.CrossRefPubMedGoogle Scholar
  173. Yuval-Greenberg, S., Merriam, E. P., & Heeger, D. J. (2014). Spontaneous microsaccades reflect shifts in covert attention. The Journal of Neuroscience, 34(41), 13693–13700.  https://doi.org/10.1523/jneurosci.0582-14.2014.CrossRefPubMedPubMedCentralGoogle Scholar
  174. Zuber, B. L., & Stark, L. (1965). Microsaccades and the velocityamplitude relationship for saccadic eye movements. Science, 150, 1459–1460.Google Scholar

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Authors and Affiliations

  1. 1.State University of New York Downstate Health Sciences UniversityBrooklynUSA

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