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.

Improved visual sensitivity during smooth pursuit eye movements

Nature Neuroscience volume 11, pages 1211–1216 (2008)Cite this article

Abstract

When we view the world around us, we constantly move our eyes. This brings objects of interest into the fovea and keeps them there, but visual sensitivity has been shown to deteriorate while the eyes are moving. Here we show that human sensitivity for some visual stimuli is improved during smooth pursuit eye movements. Detection thresholds for briefly flashed, colored stimuli were 16% lower during pursuit than during fixation. Similarly, detection thresholds for luminance-defined stimuli of high spatial frequency were lowered. These findings suggest that the pursuit-induced sensitivity increase may have its neuronal origin in the parvocellular retino-thalamic system. This implies that the visual system not only uses feedback connections to improve processing for locations and objects being attended to, but that a whole processing subsystem can be boosted. During pursuit, facilitation of the parvocellular system may reduce motion blur for stationary objects and increase sensitivity to speed changes of the tracked object.

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

Get just this article for as long as you need it

$39.95

Learn more

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

Figure 1: Experimental protocol.
Figure 2: Contrast thresholds during pursuit and fixation for red-green color and luminance stimuli.
Figure 3: Influence of spatial location and stimulus type.
Figure 4: Influence of temporal and spatial integration.
Figure 5: Influence of pursuit velocity.
Figure 6: Dynamics of the enhancement.

References

  1. Martinez-Conde, S., Macknik, S.L. & Hubel, D.H. The role of fixational eye movements in visual perception. Nat. Rev. Neurosci. 5, 229–240 (2004).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  3. Burr, D.C., Morrone, M.C. & Ross, J. Selective suppression of the magnocellular visual pathway during saccadic eye movements. Nature 371, 511–513 (1994).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  5. Morrone, M.C., Ross, J. & Burr, D. Saccadic eye movements cause compression of time as well as space. Nat. Neurosci. 8, 950–954 (2005).

    Article  CAS  Google Scholar 

  6. Khurana, B. & Kowler, E. Shared attentional control of smooth eye movement and perception. Vision Res. 27, 1603–1618 (1987).

    Article  CAS  Google Scholar 

  7. Kerzel, D. & Ziegler, N.E. Visual short-term memory during smooth pursuit eye movements. J. Exp. Psychol. Hum. Percept. Perform. 31, 354–372 (2005).

    Article  Google Scholar 

  8. Turano, K.A. & Heidenreich, S.M. Eye movements affect the perceived speed of visual motion. Vision Res. 39, 1177–1187 (1999).

    Article  CAS  Google Scholar 

  9. Kerzel, D., Aivar, M.P., Ziegler, N.E. & Brenner, E. Mislocalization of flashes during smooth pursuit hardly depends on the lighting conditions. Vision Res. 46, 1145–1154 (2006).

    Article  Google Scholar 

  10. Schütz, A.C., Delipetkos, E., Braun, D.I., Kerzel, D. & Gegenfurtner, K.R. Temporal contrast sensitivity during smooth pursuit eye movements. J. Vis. 7, 3.1–3.15 (2007).

    Article  Google Scholar 

  11. Derrington, A.M., Krauskopf, J. & Lennie, P. Chromatic mechanisms in lateral geniculate nucleus of macaque. J. Physiol. (Lond.) 357, 241–265 (1984).

    Article  CAS  Google Scholar 

  12. Levitt, H. Transformed up-down methods in psychoacoustics. J. Acoust. Soc. Am. 49, 467–477 (1971).

    Article  Google Scholar 

  13. Krauzlis, R.J. & Lisberger, S.G. Temporal properties of visual motion signals for the initiation of smooth pursuit eye movements in monkeys. J. Neurophysiol. 72, 150–162 (1994).

    Article  CAS  Google Scholar 

  14. Lisberger, S.G., Morris, E.J. & Tychsen, L. Visual motion processing and sensory-motor integration for smooth pursuit eye movements. Annu. Rev. Neurosci. 10, 97–129 (1987).

    Article  CAS  Google Scholar 

  15. Gegenfurtner, K.R. et al. Chromatic properties of neurons in macaque MT. Vis. Neurosci. 11, 455–466 (1994).

    Article  CAS  Google Scholar 

  16. Gegenfurtner, K.R. & Hawken, M.J. Interaction of motion and color in the visual pathways. Trends Neurosci. 19, 394–401 (1996).

    Article  CAS  Google Scholar 

  17. Chaparro, A., Stromeyer, C.F. III, Huang, E.P., Kronauer, R.E. & Eskew, R.T. Jr. Colour is what the eye sees best. Nature 361, 348–350 (1993).

    Article  CAS  Google Scholar 

  18. Schiller, P.H., Logothetis, N.K. & Charles, E.R. Functions of the colour-opponent and broad-band channels of the visual system. Nature 343, 68–70 (1990).

    Article  CAS  Google Scholar 

  19. Merigan, W.H., Katz, L.M. & Maunsell, J.H. The effects of parvocellular lateral geniculate lesions on the acuity and contrast sensitivity of macaque monkeys. J. Neurosci. 11, 994–1001 (1991).

    Article  CAS  Google Scholar 

  20. Casagrande, V.A. A third parallel visual pathway to primate area V1. Trends Neurosci. 17, 305–310 (1994).

    Article  CAS  Google Scholar 

  21. Nishida, S., Watanabe, J., Kuriki, I. & Tokimoto, T. Human visual system integrates color signals along a motion trajectory. Curr. Biol. 17, 366–372 (2007).

    Article  CAS  Google Scholar 

  22. Schwartz, J.D. & Lisberger, S.G. Initial tracking conditions modulate the gain of visuo-motor transmission for smooth pursuit eye movements in monkeys. Vis. Neurosci. 11, 411–424 (1994).

    Article  CAS  Google Scholar 

  23. Tanaka, M. & Lisberger, S.G. Regulation of the gain of visually guided smooth-pursuit eye movements by frontal cortex. Nature 409, 191–194 (2001).

    Article  CAS  Google Scholar 

  24. Van Donkelaar, P. & Drew, A.S. The allocation of attention during smooth pursuit eye movements. Prog. Brain Res. 140, 267–277 (2002).

    Article  Google Scholar 

  25. Ilg, U.J. & Thier, P. Inability of rhesus monkey area V1 to discriminate between self-induced and externally induced retinal image slip. Eur. J. Neurosci. 8, 1156–1166 (1996).

    Article  CAS  Google Scholar 

  26. von Holst, E. & Mittelstaed, E. Das Reafferenzprinzip. Naturwissenschaften 37, 464–475 (1950).

    Article  Google Scholar 

  27. Burr, D.C. & Morrone, M.C. Temporal impulse response functions for luminance and colour during saccades. Vision Res. 36, 2069–2078 (1996).

    Article  CAS  Google Scholar 

  28. Ramachandran, V.S. Perception of shape from shading. Nature 331, 163–166 (1988).

    Article  CAS  Google Scholar 

  29. Hansen, T., Olkkonen, M., Walter, S. & Gegenfurtner, K.R. Memory modulates color appearance. Nat. Neurosci. 9, 1367–1368 (2006).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  31. Ilg, U.J., Schumann, S. & Thier, P. Posterior parietal cortex neurons encode target motion in world-centered coordinates. Neuron 43, 145–151 (2004).

    Article  CAS  Google Scholar 

  32. Ilg, U.J. & Thier, P. Visual tracking neurons in primate area MST are activated by smooth-pursuit eye movements of an “imaginary” target. J. Neurophysiol. 90, 1489–1502 (2003).

    Article  Google Scholar 

  33. Ono, S. & Mustari, M.J. Extraretinal signals in MSTd neurons related to volitional smooth pursuit. J. Neurophysiol. 96, 2819–2825 (2006).

    Article  Google Scholar 

  34. Freeman, T.C. Extra-retinal vision: firing at will. Curr. Biol. 17, R99–R101 (2007).

    Article  CAS  Google Scholar 

  35. Tanaka, M. & Lisberger, S.G. Role of arcuate frontal cortex of monkeys in smooth pursuit eye movements. I. Basic response properties to retinal image motion and position. J. Neurophysiol. 87, 2684–2699 (2002).

    Article  Google Scholar 

  36. Osborne, L.C., Hohl, S.S., Bialek, W. & Lisberger, S.G. Time course of precision in smooth-pursuit eye movements of monkeys. J. Neurosci. 27, 2987–2998 (2007).

    Article  CAS  Google Scholar 

  37. Bedell, H.E. & Lott, L.A. Suppression of motion-produced smear during smooth pursuit eye movements. Curr. Biol. 6, 1032–1034 (1996).

    Article  CAS  Google Scholar 

  38. Tong, J., Aydin, M. & Bedell, H.E. Direction and extent of perceived motion smear during pursuit eye movement. Vision Res. 47, 1011–1019 (2007).

    Article  Google Scholar 

  39. Segraves, M.A. & Goldberg, M.E. Effect of stimulus position and velocity upon the maintenance of smooth pursuit eye velocity. Vision Res. 34, 2477–2482 (1994).

    Article  CAS  Google Scholar 

  40. Blohm, G., Missal, M. & Lefevre, P. Direct evidence for a position input to the smooth pursuit system. J. Neurophysiol. 94, 712–721 (2005).

    Article  Google Scholar 

  41. Perrone, J.A. & Thiele, A. Speed skills: measuring the visual speed analyzing properties of primate MT neurons. Nat. Neurosci. 4, 526–532 (2001).

    Article  CAS  Google Scholar 

  42. Mikami, A., Newsome, W.T. & Wurtz, R.H. Motion selectivity in macaque visual cortex. I. Mechanisms of direction and speed selectivity in extrastriate area MT. J. Neurophysiol. 55, 1308–1327 (1986).

    Article  CAS  Google Scholar 

  43. Newsome, W.T., Wurtz, R.H., Dursteler, M.R. & Mikami, A. Deficits in visual motion processing following ibotenic acid lesions of the middle temporal visual area of the macaque monkey. J. Neurosci. 5, 825–840 (1985).

    Article  CAS  Google Scholar 

  44. Wilmer, J.B. & Nakayama, K. Two distinct visual motion mechanisms for smooth pursuit: evidence from individual differences. Neuron 54, 987–1000 (2007).

    Article  CAS  Google Scholar 

  45. Seiffert, A.E. & Cavanagh, P. Position-based motion perception for color and texture stimuli: effects of contrast and speed. Vision Res. 39, 4172–4185 (1999).

    Article  CAS  Google Scholar 

  46. Segraves, M.A. et al. The role of striate cortex in the guidance of eye movements in the monkey. J. Neurosci. 7, 3040–3058 (1987).

    Article  CAS  Google Scholar 

  47. Krauzlis, R.J., Basso, M.A. & Wurtz, R.H. Shared motor error for multiple eye movements. Science 276, 1693–1695 (1997).

    Article  CAS  Google Scholar 

  48. Schütz, A.C., Braun, D.I. & Gegenfurtner, K.R. Contrast sensitivity during the initiation of smooth pursuit eye movements. Vision Res. 47, 2767–2777 (2007).

    Article  Google Scholar 

  49. Wyatt, H.J. Detecting saccades with jerk. Vision Res. 38, 2147–2153 (1998).

    Article  CAS  Google Scholar 

  50. Wichmann, F.A. & Hill, N.J. The psychometric function: I. Fitting, sampling, and goodness of fit. Percept. Psychophys. 63, 1293–1313 (2001).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank M. Hawken and M. Spering for comments and suggestions, U. Kleinholderman and W. Kirchner for technical assistance and S. Bader, M. Höfer and E. Baumgartner for help with data collection. This work was supported by the German Research Foundation Forschergruppe “Perception and Action” and the German Research Foundation Graduiertenkolleg “NeuroAct”.

Author information

Authors and Affiliations

  1. Abteilung Allgemeine Psychologie, Justus-Liebig-Universität Giessen, Otto-Behaghel-Strasse 10F, Giessen, D-35394, Germany

    Alexander C Schütz, Doris I Braun & Karl R Gegenfurtner

  2. Faculté de Psychologie et des Sciences de l'Education, Université de Genève, 40 Boulevard du Pont d'Arve, Genève, CH-1205, Switzerland

    Dirk Kerzel

Authors
  1. Alexander C Schütz
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Doris I Braun
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Dirk Kerzel
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Karl R Gegenfurtner
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Karl R Gegenfurtner.

Supplementary information

Supplementary Text and Figures

Supplementary Figures 1–4 and Supplementary Note (PDF 212 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Schütz, A., Braun, D., Kerzel, D. et al. Improved visual sensitivity during smooth pursuit eye movements. Nat Neurosci 11, 1211–1216 (2008). https://doi.org/10.1038/nn.2194

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nn.2194

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