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.

  • Review Article
  • Published:

Through the eye, slowly; Delays and localization errors in the visual system

Key Points

  • Afferent delays in the visual system are long and often lead to the mislocalization of objects. When our eyes or visible objects move, temporal errors in transmitting and processing neural signals can easily translate into spatial errors. This review considers three cases in which this occurs: when we pursue a moving target, when we try to localize a target that is presented just before a saccadic eye movement, and when we try to locate a moving stimulus with respect to a flashed one.

  • During smooth pursuit, an image of the moving target is always on the fovea. However, when that image reaches the level of perception, the eye is already pointing further along the anticipated target trajectory. Therefore, 'what-we-see' might not correspond to 'where-we-are-looking-at-that-instant'. Experimental data indicate that this is indeed the case. If so, our brain does not attempt to compensate for visual afferent delays.

  • The delay problem encountered in smooth pursuit is exacerbated during saccades because they are so fast. A large saccade can be performed during the time it takes for the image of a flashed object to reach the level of perception. How, then, can we localize the object? In the absence of any other visual cue, we have to rely on internal information about the trajectory and time course of the performed saccade. Experimental data show that this information (called the eye-position signal, or EPS) is available, although it is quite distorted. The distortion causes systematic mislocalizations, which affect stimuli presented not only during a saccade, but also before and after, when the eye is stable.

  • A number of illusions caused by stimulus motion are strikingly similar to perisaccadic mislocalization. The best known is the flash-lag effect, in which the perceived spatial relationship between a moving object and a stable one that is briefly flashed in the dark seems to be distorted. We argue that the cause of the illusion might be the indeterminacy of the exact time of an event (such as the flash). Recent data show that our current models of peaks of activity in visual maps are too simplistic to account for localization in the presence of change.

  • Analogous misperceptions can occur with other types of change, apart from stimulus–retinal slip. The problem can be formulated in general terms: when a variable changes (eye, body or stimulus variable), even predictably, how does the brain determine its state at the instant specified by an event? To answer this question, we have to understand how the brain encodes a changing variable (for example, position versus velocity signals), and how it reads that code (continuously or by sampling).

Abstract

Reviews on the visual system generally praise its amazing performance. Here we deal with its biggest weakness: sluggishness. Inherent delays lead to mislocalization when things move or, more generally, when things change. Errors in time translate into spatial errors when we pursue a moving object, when we try to localize a target that appears just before a gaze shift, or when we compare the position of a flashed target with the instantaneous position of a continuously moving one (or one that appears to be moving even though no change occurs in the retinal image). Studying such diverse errors might rekindle our thinking about how the brain copes with real-time changes in the world.

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

Access options

Buy this article

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

Figure 1: Effect of visual delay in smooth pursuit.
Figure 2: Interconnections between oculomotor centres for saccades and smooth pursuit.
Figure 3: Layout of the double-step task.
Figure 4: Steps involved in determining the time course of the hypothetical eye-position signal.
Figure 5: Nijhawan's flash-lag set-up.
Figure 6: Flash-lag induced by rotation in a vestibular chair.

Similar content being viewed by others

References

  1. Hazelhoff, F. & Wiersma, H. Die Wahrnehmungszeit. Z. Psychol. 96, 181–188 (1924).

    Google Scholar 

  2. Schmolesky, M. T. et al. Signal timing across the macaque visual system. J. Neurophysiol. 79, 3272–3278 (1998).

    CAS  PubMed  Google Scholar 

  3. Ward, F. in Eye Movements and Psychological Processes (eds Monty, R. A. & Senders, J. W.) 289–297 (Erlbaum, Hillsdale, New Jersey, 1976).

    Google Scholar 

  4. Mateeff, S., Yakimoff, N. & Dimitrov, G. Localization of brief stimuli during pursuit eye movements. Acta Psychol. (Amst.) 48, 133–140 (1981).

    CAS  Google Scholar 

  5. Brenner E., Smeets, J. B. J. & van den Berg, A. V. Smooth eye movements and spatial localisation. Vision Res. 41, 2253–2259 (2001).

    CAS  PubMed  Google Scholar 

  6. Smeets, J. B. J. & Brenner, E. Perception and action are based on the same visual information: distinction between position and velocity. J. Exp. Psychol. Hum. Percept. Perform. 21, 19–31 (1995).

    CAS  PubMed  Google Scholar 

  7. Newsome, W. T., Wurtz, R. H. & Komatsu, H. Relation of cortical areas MT and MST to pursuit eye movements. II. Differentiation of retinal from extraretinal inputs. J. Neurophysiol. 60, 604–620 (1988).

    CAS  PubMed  Google Scholar 

  8. Paillard, J. Quelques données psychophysiologiques relatives au déclenchement de la commande motrice. Année Psychol. 48, 28–47 (1948).

    Google Scholar 

  9. Aschersleben, G. & Prinz, W. Synchronizing actions with events: the role of sensory information. Percept. Psychophys. 57, 305–317 (1995).

    CAS  PubMed  Google Scholar 

  10. Aschersleben, G. in Cognitive Contributions to the Perception of Spatial and Temporal Events (eds Aschersleben, G., Bachmann, T. & Müsseler, J.) 293–318 (Elsevier, Amsterdam, 1999).

    Google Scholar 

  11. Churchland, M. M. & Lisberger, S. G. Experimental and computational analysis of monkey smooth pursuit eye movements. J. Neurophysiol. 86, 741–759 (2001).

    CAS  PubMed  Google Scholar 

  12. Dassonville, P., Schlag, J. & Schlag-Rey, M. Oculomotor localization relies on a damped representation of saccadic eye displacement in human and nonhuman primates. Vis. Neurosci. 9, 261–269 (1992).

    CAS  PubMed  Google Scholar 

  13. Dassonville, P., Schlag, J. & Schlag-Rey, M. Direction constancy in the oculo-motor system. Curr. Dir. Psychol. Sci. 2, 143–147 (1993).

    Google Scholar 

  14. Mitrani, L., Mateeff, S. & Yakimoff, N. Smearing of the retinal image during voluntary saccadic eye movements. Vision Res. 10, 405–409 (1970).

    CAS  PubMed  Google Scholar 

  15. Matin, L. & Pearce, D. G. Visual perception of direction for stimuli flashed during voluntary saccadic eye movement. Science 148, 1485–1488 (1965).Although not the first one on this topic, this is the most influential paper to have drawn attention to mislocalization near the time of saccades.

    CAS  PubMed  Google Scholar 

  16. Bischof, F. & Kramer, E. Untersuchungen und Überlegungen zur Richtungswahrnehmung bei willkürlichen sakkadischen Augenbewegungen. Psychol. Forsch. 32, 185–218 (1968).

    CAS  PubMed  Google Scholar 

  17. Hallett, P. E. & Lightstone, A. D. Saccadic eye movements toward stimuli triggered by prior saccades. Vision Res. 16, 99–106 (1976).This study provided evidence that the brain uses an EPS to locate visual targets in the dark.

    CAS  PubMed  Google Scholar 

  18. Hansen, R. M. & Skavenski, A. A. Accuracy of spatial localization near the time of saccadic eye movements. Vision Res. 25, 1077–1082 (1985).

    CAS  PubMed  Google Scholar 

  19. Honda, H. Spatial localization in saccade and pursuit-eye-movement conditions: a comparison of perceptual and motor measures. Percept. Psychophys. 38, 41–46 (1985).

    CAS  PubMed  Google Scholar 

  20. Honda, H. in Attention and Performance XIII: Motor Representation and Control. (ed. Jeannerod, M.) 567–582 (Erlbaum, Hillsdale, New Jersey, 1990).

    Google Scholar 

  21. Dassonville, P., Schlag, J. & Schlag-Rey, M. The use of egocentric and exocentric location cues in saccadic programming. Vision Res. 35, 2191–2199 (1995).

    CAS  PubMed  Google Scholar 

  22. Schlag, J. & Schlag-Rey, M. Illusory localization of stimuli flashed in the dark before saccades. Vision Res. 35, 2347–2357 (1995).

    CAS  PubMed  Google Scholar 

  23. Bockisch, C. J. & Miller, J. M. Different motor systems use similar damped extraretinal eye position information. Vision Res. 39, 1025–1038 (1999).

    CAS  PubMed  Google Scholar 

  24. Matin, L. et al. Oculoparalytic illusion: visual-field dependent spatial mislocalizations by humans partially paralyzed with curare. Science 216, 198–201 (1982).Probably the most elegant demonstration of the role of the internal EPS in stimulus localization and of its overriding by ambient visual cues.

    CAS  PubMed  Google Scholar 

  25. Bridgeman, B. & Delgado, D. Sensory effects of eye press are due to efference. Percept. Psychophys. 36, 482–484 (1984).

    CAS  PubMed  Google Scholar 

  26. Grüsser, O.-J., Krizic, A. & Weiss, L.-R. After-image movement during saccades in dark. Vision Res. 27, 215–226 (1987).

    PubMed  Google Scholar 

  27. Mergner, T., Nasios, G., Maurer, C. & Becker, W. Visual localization in space: interaction of retinal, eye position, vestibular and neck proprioceptive information. Exp. Brain Res. 141, 33–51 (2001).

    CAS  PubMed  Google Scholar 

  28. Goldberg, M. E. & Bruce, C. J. Primate frontal eye fields. III. Maintenance of spatially accurate saccade signal. J. Neurophysiol. 64, 489–508 (1990).

    CAS  PubMed  Google Scholar 

  29. Moschovakis, A. K., Karalelas, A. B. & Highstein, S. N. Structure–function relationships in the primate superior colliculus. II. Morphological identity of presaccadic neurons. J. Neurophysiol. 60, 263–302 (1988).

    CAS  PubMed  Google Scholar 

  30. Quaia, C., Optican, L. M. & Goldberg, M. E. The maintenance of spatial accuracy by the perisaccadic remapping of visual receptive fields. Neural Netw. 11, 1229–1240 (1998).

    PubMed  Google Scholar 

  31. Zipser, D. & Andersen, R. A. A back-propagation programmed network that stimulates response properties of a subset of posterior parietal neurons. Nature 331, 679–684 (1988).

    CAS  PubMed  Google Scholar 

  32. Duhamel, J.-R., Colby, C. L. & Goldberg, M. E. The updating of the representation of visual space in parietal cortex by intended eye movements. Science 255, 90–92 (1992).

    CAS  PubMed  Google Scholar 

  33. Umeno, M. M. & Goldberg, M. E. Spatial processing in the monkey's frontal eye field. Predictive visual responses. J. Neurophysiol. 78, 1373–1383 (1997).

    CAS  PubMed  Google Scholar 

  34. Walker, M. F., FitzGibbon, E. J. & Goldberg, M. E. Neurons in the monkey superior colliculus predict the result of impending saccadic eye movements. J. Neurophysiol. 73, 1988–2003 (1995).

    CAS  PubMed  Google Scholar 

  35. Honda, H. Perceptual localization of visual stimuli flashed during saccades. Percept. Psychophys. 45, 162–174 (1989).

    CAS  PubMed  Google Scholar 

  36. Boucher, L., Groh, J. M. & Hughes, H. C. Afferent delays and the mislocalization of perisaccadic stimuli. Vision Res. 41, 2631–2644 (2001).

    CAS  PubMed  Google Scholar 

  37. Pouget, A., Albright, T. & Sejnowski, T. A dynamic model for computing the position of an object from its retinal location and eye position. Soc. Neurosci. Abstr. 18, 1396 (1992).

  38. Pola, J. R & Wyatt, H. J. The time course of the extraretinal signal for saccade-contingent perceived direction may be as fast as the saccade. Soc. Neurosci. Abstr. 31, 58.19 (2001).

    Google Scholar 

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

    Google Scholar 

  40. Volkmannn, F. C. & Moore, R. K. in Visual Psychophysics and Physiology (eds Armington, J. C., Krauskopf, J. & Wooden, B. R.) 353–362 (Academic, New York, 1978).

    Google Scholar 

  41. Dassonville, P. Haptic localization and internal representation of the hand in space. Exp. Brain Res. 106, 434–448 (1995).

    CAS  PubMed  Google Scholar 

  42. Hershberger, W. Saccadic eye movements and the perception of visual direction. Percept. Psychophys. 41, 35–44 (1987).

    CAS  PubMed  Google Scholar 

  43. Kubischik, M. & Bremmer, F. Peri-saccadic space representation in monkey inferior parietal cortex. Soc. Neurosci. Abstr. 25, 1164 (1999).

    Google Scholar 

  44. Mays, L. E. & Sparks, D. L. Dissociation of visual and saccade-related responses in superior colliculus neurons. J. Neurophysiol. 43, 207–232 (1980).

    CAS  PubMed  Google Scholar 

  45. Robinson, D. A. & Fuchs, A. F. Eye movements evoked by stimulation of frontal eye fields. J. Neurophysiol. 32, 637–648 (1969).

    CAS  PubMed  Google Scholar 

  46. Sparks, D. L. & Mays, L. E. Spatial localization of saccade targets. I. Compensation for stimulus induced perturbations in eye position. J. Neurophysiol. 49, 45–74 (1983).

    CAS  PubMed  Google Scholar 

  47. Schlag, J. & Schlag-Rey, M. Does microstimulation evoke fixed vector saccades by generating their vector or by specifying their goal? Exp. Brain Res. 68, 442–444 (1987).

    CAS  PubMed  Google Scholar 

  48. Schlag, J. & Schlag-Rey, M. Colliding saccades may reveal the secret of their marching orders. Trends Neurosci. 13, 410–415 (1990).

    CAS  PubMed  Google Scholar 

  49. Dassonville, P., Schlag, J. & Schlag-Rey, M. The frontal eye field provides the goal of saccadic eye movement. Exp. Brain Res. 89, 300–310 (1992).

    CAS  PubMed  Google Scholar 

  50. Schlag, J., Schlag-Rey, M. & Dassonville, P. Interactions between natural and electrically evoked saccades. II. At what time is eye position sampled as a reference for the localization of a target? Exp. Brain Res. 76, 548–558 (1989).

    CAS  PubMed  Google Scholar 

  51. Schlag-Rey, M., Schlag, J. & Dassonville, P. Interactions between natural and electrically evoked saccades. I. Differences between sites carrying retinal error and motor command signals in monkey superior colliculus. Exp. Brain Res. 76, 537–547 (1989).

    CAS  PubMed  Google Scholar 

  52. Dominey, P. F., Schlag, J., Schlag-Rey, M. & Arbib, M. A. Colliding saccades evoked by frontal eye field stimulation: artifact or evidence for an oculomotor compensatory mechanism underlying double-step saccades. Biol. Cybern. 76, 41–52 (1997).

    CAS  PubMed  Google Scholar 

  53. Brenner, E. & Cornelissen, F. W. Separate simultaneous processing of egocentric and relative positions. Vision Res. 40, 2557–2564 (2000).

    CAS  PubMed  Google Scholar 

  54. Honda, H. Saccade-contingent displacement of the apparent position of visual stimuli flashed on a dimly illuminated structured background. Vision Res. 33, 709–716 (1993).

    CAS  PubMed  Google Scholar 

  55. Karn, K. S., Moller, P. & Hayhoe, M. M. Reference frames in saccadic targeting. Exp. Brain Res. 115, 267–282 (1997).

    CAS  PubMed  Google Scholar 

  56. Hahnloser, R., Douglas, R. G., Mahowald, M. & Hepp, K. Feedback interactions between neuronal pointers and maps for attentional processing. Nature Neurosci. 2, 746–752 (1999).

    CAS  PubMed  Google Scholar 

  57. Cai, R. H., Pouget, A., Schlag-Rey, M. & Schlag, J. Perceived geometrical relationships affected by eye-movement signals. Nature 386, 601–604 (1997).

    CAS  PubMed  Google Scholar 

  58. Ross, J., Morrone, M. C. & Burr, D. C. Compression of visual space before saccades. Nature 386, 598–601 (1997).

    CAS  PubMed  Google Scholar 

  59. Morrone, M. C., Ross, J. & Burr, D. C. Apparent position of visual targets during real and simulated saccadic eye movements. J. Neurosci. 17, 7941–7953 (1997).

    CAS  PubMed  PubMed Central  Google Scholar 

  60. Lappe, M., Awater, H. & Krekelberg, B. Postsaccadic visual references generate presaccadic compression of space. Nature 403, 892–895 (2000).

    CAS  PubMed  Google Scholar 

  61. 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).

    CAS  PubMed  Google Scholar 

  62. van Beers, R. J., Wolpert, D. M. & Haggard, P. Sensorimotor integration compensates for visual localization errors during smooth pursuit eye movements. J. Neurophysiol. 85, 1914–1922 (2001).

    CAS  PubMed  Google Scholar 

  63. Deubel, H., Schneider, W. X. & Bridgeman, B. Postsaccadic target blanking prevents saccadic suppression of image displacement. Vision Res. 36, 985–996 (1996).

    CAS  PubMed  Google Scholar 

  64. Fröhlich, F. W. Über die Messung der Empfindungszeit. Z. Sinnesphysiol. 54, 57–78 (1923).

    Google Scholar 

  65. Metzger, W. Versuch einer gemeinsamen Theorie der Phänomene Fröhlichs und Hazelhoffs und Kritik ihrer Vefahren zur Messung der Empfindungszeit. Psychol. Forsch. 16, 176–200 (1931).

    Google Scholar 

  66. MacKay, D. M. Perceptual stability of a stroboscopically lit visual field containing self-luminous objects. Nature 181, 507–508 (1958).

    CAS  PubMed  Google Scholar 

  67. Nijhawan, R. Motion extrapolation in catching. Nature 370, 256–257 (1994).This short paper renewed interest in the flash-lag phenomenon and started an intense debate.

    CAS  PubMed  Google Scholar 

  68. Nijhawan, R. The flash-lag phenomenon: object motion and eye movements. Perception 30, 263–282 (2001).

    CAS  PubMed  Google Scholar 

  69. Purushothaman, G., Patel, S. S., Bedell, H. E. & Ogmen, H. Moving ahead through differential visual latency. Nature 396, 424 (1998).

    CAS  PubMed  Google Scholar 

  70. Whitney, D. & Murakami, I. Latency difference, not spatial extrapolation. Nature Neurosci. 1, 656–657 (1998).

    CAS  PubMed  Google Scholar 

  71. Whitney, D., Murakami, I. & Cavanagh, P. Illusory spatial offset of a flash relative to a moving stimulus is caused by differential latencies for moving and flashed stimuli. Vision Res. 40, 137–149 (2000).

    CAS  PubMed  Google Scholar 

  72. Murakami, I. A flash-lag effect in random motion. Vision Res. 41, 3101–3119 (2001).

    CAS  PubMed  Google Scholar 

  73. Baldo, M. V. C. & Klein, S. A. Extrapolation or attention shift? Nature 378, 565–566 (1995).

    CAS  PubMed  Google Scholar 

  74. Super, H., Spekreijse, H. & Lamme, V. A. F. Two distinct modes of sensory processing observed in monkey primary visual cortex (V1). Nature Neurosci. 4, 304–310 (2001).

    CAS  PubMed  Google Scholar 

  75. Allik, J. & Kreegipuu, K. Multiple visual latency. Psychol. Sci. 9, 135–138 (1998).

    Google Scholar 

  76. Arnold, D. H., Clifford, C. W. G. & Wenderoth, P. Asynchronous processing in vision: color leads motion. Curr. Biol. 11, 596–600 (2001).

    CAS  PubMed  Google Scholar 

  77. Bartels, A. & Zeki, S. The theory of multistage integration in the visual brain. Proc. R. Soc. Lond. B 265, 2327–2332 (1998).

    CAS  Google Scholar 

  78. Berry, M. J., Brivanlou, I. H., Jordan, T. A. & Meister, M. Anticipation of moving stimuli by the retina. Nature 398, 334–338 (1999).

    CAS  PubMed  Google Scholar 

  79. Müller, K., Aschersleben, G., Koch, R., Freund, H. & Prinz, W. in Cognitive Contributions to the Perception of Spatial and Temporal Events (eds Aschersleben, G., Bachmann, T. & Müsseler, J.) 233–250 (Elsevier, Amsterdam, 1999)

    Google Scholar 

  80. Lappe, M. & Krekelberg, B. The position of moving objects. Perception 27, 1437–1449 (1998).

    CAS  PubMed  Google Scholar 

  81. Krekelberg, B. & Lappe, M. Temporal recruitment along the trajectory of moving objects and the perception of position. Vision Res. 39, 2669–2679 (1999).

    CAS  PubMed  Google Scholar 

  82. Watanabe, K., Nijhawan, R., Khurana, B. & Shimojo, S. Perceptual organization of moving stimuli modulates the flash-lag effect. J. Exp. Psychol. Hum. Percept. Perform. 27, 879–894 (2001).

    PubMed  Google Scholar 

  83. Brenner, E. & Smeets, J. B. J. Motion extrapolation is not responsible for the flash-lag effect. Vision Res. 40, 1645–1648 (2000).

    CAS  PubMed  Google Scholar 

  84. Eagleman, D. M. & Sejnowski, T. J. Motion integration and postdiction in visual awareness. Science 287, 2036–2038 (2000).

    CAS  PubMed  Google Scholar 

  85. Cai, R. H. & Schlag, J. Asynchronous feature binding and the flash-lag illusion. Invest. Ophthalmol. Vis. Sci. 42, 3830 (2001).

    Google Scholar 

  86. Cai, R. H., Schlag-Rey, M. & Schlag, J. Displacement of the moving bar exists in the flash-lag effect. Soc. Neurosci. Abstr. 26, 1502 (2000).

    Google Scholar 

  87. Snowden, R. J. Shifts in perception following adaptation to visual motion. Curr. Biol. 8, 1343–1345 (1998).

    CAS  PubMed  Google Scholar 

  88. Schlag, J., Cai, R. H., Dorfman, A., Mohempour, A. & Schlag-Rey, M. Extrapolating movement without retinal motion. Nature 403, 38–39 (2000).

    CAS  PubMed  Google Scholar 

  89. Cai, R. H., Jacobson, K., Baloh, R., Schlag-Rey, M. & Schlag, J. Vestibular signals can distort the perceived spatial relationship of retinal stimuli. Exp. Brain Res. 135, 275–278 (2000).

    CAS  PubMed  Google Scholar 

  90. Bachman, T. & Poder, E. Change in feature space is not necessary for the flash-lag effect. Vision Res. 41, 1103–1106 (2001).

    Google Scholar 

  91. Sheth, B., Nijhawan, R. & Shimojo, S. Changing objects lead briefly flashed ones. Nature Neurosci. 3, 489–495 (2000).

    CAS  PubMed  Google Scholar 

  92. Fu, Y.-X., Shen, Y. & Dan, Y. Motion-induced perceptual extrapolation of blurred visual targets. J. Neurosci. 21, RC172 (2001).

    CAS  PubMed  PubMed Central  Google Scholar 

  93. Deubel, H., Irwin, D. E. & Schneider, W. X. in Current Oculomotor Research: Physiological and Psychological Aspects (eds Becker, W., Deubel, H. & Mergner, T.) 65–70 (Plenum, New York, 1999).

    Google Scholar 

  94. Krekelberg, B. The persistence of position. Vision Res. 41, 529–539 (2001).

    CAS  PubMed  Google Scholar 

  95. Krekelberg, B. & Lappe, M. Neuronal latencies and the position of moving objects. Trends Neurosci. 24, 335–339 (2001).

    CAS  PubMed  Google Scholar 

  96. Tolias, A. S. et al. Eye movements modulate visual receptive fields of V4 neurons. Neuron 29, 757–767 (2001).

    CAS  PubMed  Google Scholar 

  97. Paillard, J. & Amblard, B. in Brain Mechanisms and Spatial Vision (eds Ingle, D. J., Jeannerod, M. & Lee, D. N.) 299–329 (Martinus Nijhoof, Dordrecht, 1985).

    Google Scholar 

  98. Priebe, N. J., Churchland, M. M. & Lisberger, S. G. Reconstruction of target speed for the guidance of pursuit eye movements. J. Neurosci. 21, 3196–3206 (2001).

    CAS  PubMed  PubMed Central  Google Scholar 

  99. Krekelberg, B. & Lappe, M. A model of the perceived relative positions of moving objects based upon a slow averaging process. Vision Res. 40, 201–215 (2000).

    CAS  PubMed  Google Scholar 

  100. Rao, R. P. N., Eagleman, D. M. & Sejnowski, T. J. Optimal smoothing in visual motion perception. Neural Comput. 13, 1243–1253 (2001).

    CAS  PubMed  Google Scholar 

  101. Van der Heiden, A. H. C., Müsseler, J. & Bridgeman, B. in Cognitve Contributions to the Perception of Spatial and Temporal Events (eds Aschersleben, G., Bachmann, T. & Müsseler, J.) 19–37 (Elsevier, Amsterdam, 1999).

    Google Scholar 

  102. De Valois, R. L. & De Valois, K. K. Vernier acuity with stationary moving Gabors. Vision Res. 31, 1619–1626 (1991).

    CAS  PubMed  Google Scholar 

  103. Nishida, S. & Johnston, A. Influence of motion signals on the perceived position of spatial pattern. Nature 397, 610–612 (1999).

    CAS  PubMed  Google Scholar 

  104. Whitney, D. & Cavanagh, P. Motion distorts visual space: shifting the perceived position of remote stationary objects. Nature Neurosci. 3, 954–959 (2000).

    CAS  PubMed  Google Scholar 

  105. Tian, J.-R. & Lynch, J. C. Corticocortical input to the smooth and saccadic eye movement subregions of the frontal eye field in Cebus monkeys. J. Neurophysiol. 76, 2754–2771 (1996).

    CAS  PubMed  Google Scholar 

  106. Andersen, R. A., Asanuma, C., Essick, G. & Siegel, R. M. Corticocortical connections of anatomically and physiologically defined subdivisions within the inferior parietal lobule. J. Comp. Neurol. 296, 65–113 (1990).

    CAS  PubMed  Google Scholar 

  107. Boussaoud, D., Ungerleider, L. G. & Desimone, R. Pathways for motion analysis: cortical connections of the medial superior temporal and fundus of the superior temporal visual areas in the macaque. J. Comp. Neurol. 296, 462–495 (1990).

    CAS  PubMed  Google Scholar 

  108. Cavada, C. & Goldman-Rakic, P. S. Posterior parietal cortex in rhesus monkey. I. Parcellation of areas based on distinctive limbic and sensory corticocortical connections. J. Comp. Neurol. 287, 393–421 (1989).

    CAS  PubMed  Google Scholar 

  109. Huerta, M. F. & Kaas, J. H. Supplementary eye field as defined by intracortical microstimulation: connections in macaques. J. Comp. Neurol. 293, 299–330 (1990).

    CAS  PubMed  Google Scholar 

  110. Schall, J. D., Morel, A., King, D. J. & Bullier, J. Topography of visual cortex connections with frontal eye field in macaque: convergence and segregation of processing streams. J. Neurosci. 15, 4464–4487 (1995).

    CAS  PubMed  PubMed Central  Google Scholar 

  111. Yin, J., Schlag-Rey, M. & Schlag, J. Comparison of origins of projections from LIP to SEF and FEF in primate. Soc. Neurosci Abstr. 20, 145 (1994).

    Google Scholar 

  112. Schlag-Rey, M. & Schlag, J. in The Neurobiology of Saccadic Eye Movements (eds Wurtz, R. H. & Goldberg, M. E.) 361–390 (Elsevier, Amsterdam, 1989)

    Google Scholar 

  113. Kraulzlis, R. J. & Stone, L. S. Tracking with the mind's eye. Trends Neurosci. 22, 544–550 (1999).

    Google Scholar 

Download references

Acknowledgements

Support was provided by grants from the National Institutes of Health. We thank E. Brenner, P. Dassonville, R. Cai and J. Park for helpful comments.

Author information

Authors and Affiliations

Authors

Related links

Related links

FURTHER INFORMATION

oculomotor system

 MIT Encyclopedia of Cognitive Sciences

eye movements and visual attention

oculomotor control

spatial perception

LINKS

Nature

Glossary

CLOSED LOOP

A system in which the input is made dependent on the output by feedback.

EFFERENCE COPY

A copy of a motor command that is sent back to the central nervous system to inform it of the executed movement.

SPATIAL CONSTANCY

The perceptual assumption that objects are still where they were in the world when the retinal shift of their image is caused by our own movements.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Schlag, J., Schlag-Rey, M. Through the eye, slowly; Delays and localization errors in the visual system. Nat Rev Neurosci 3, 191 (2002). https://doi.org/10.1038/nrn750

Download citation

  • Issue date:

  • DOI: https://doi.org/10.1038/nrn750

This article is cited by

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