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Predictive remapping of attention across eye movements

Abstract

Many cells in retinotopic brain areas increase their activity when saccades (rapid eye movements) are about to bring stimuli into their receptive fields. Although previous work has attempted to look at the functional correlates of such predictive remapping, no study has explicitly tested for better attentional performance at the future retinal locations of attended targets. We found that, briefly before the eyes start moving, attention drawn to the targets of upcoming saccades also shifted to those retinal locations that the targets would cover once the eyes had moved, facilitating future movements. This suggests that presaccadic visual attention shifts serve to both improve presaccadic perceptual processing at the target locations and speed subsequent eye movements to their new postsaccadic locations. Predictive remapping of attention provides a sparse, efficient mechanism for keeping track of relevant parts of the scene when frequent rapid eye movements provoke retinal smear and temporal masking.

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Figure 1: Predictive remapping across eye movements.
Figure 2: Predictive remapping of attention in the double-step task.
Figure 3: Controlling for the spread of attention in the double-step task.
Figure 4: Controlling for cue-based facilitation in the double-step task.
Figure 5: Predictive remapping of attention to the fovea.

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References

  1. Castet, E., Jeanjean, S. & Masson, G.S. Motion perception of saccade-induced retinal translation. Proc. Natl. Acad. Sci. USA 99, 15159–15163 (2002).

    Article  CAS  Google Scholar 

  2. Mack, A. & Rock, I. Inattentional Blindness (MIT Press, Cambridge, Massachusetts, 1998).

  3. O'Regan, J.K., Rensink, R.A. & Clark, J.J. Change-blindness as a result of 'mudsplashes'. Nature 398, 34 (1999).

    Article  CAS  Google Scholar 

  4. Wurtz, R.H. Neuronal mechanisms of visual stability. Vision Res. 48, 2070–2089 (2008).

    Article  Google Scholar 

  5. Deubel, H. The time course of presaccadic attention shifts. Psychol. Res. 72, 630–640 (2008).

    Article  Google Scholar 

  6. Montagnini, A. & Castet, E. Spatiotemporal dynamics of visual attention during saccade preparation: independence and coupling between attention and movement planning. J. Vis. 7, 1–16 (2007).

    Article  Google Scholar 

  7. Deubel, H. & Schneider, W.X. Saccade target selection and object recognition: evidence for a common attentional mechanism. Vis. Res. 14, 1827–1837 (1996).

    Article  Google Scholar 

  8. Kowler, E., Anderson, E., Dosher, B. & Blaser, E. The role of attention in the programming of saccades. Vision Res. 35, 1897–1916 (1995).

    Article  CAS  Google Scholar 

  9. Baldauf, D. & Deubel, H. Properties of attentional selection during the preparation of sequential saccades. Exp. Brain Res. 184, 411–425 (2008).

    Article  Google Scholar 

  10. Gersch, T.M., Schnitzer, B.S., Sanghvi, P.S., Dosher, B. & Kowler, E. Attentional enhancement along the path of a sequence of saccades. Vis. Cogn. 14, 104–107 (2006).

    Google Scholar 

  11. Godijn, R. & Theeuwes, J. Parallel allocation of attention prior to the execution of saccade sequences. J. Exp. Psychol. Hum. Percept. Perform. 29, 882–896 (2003).

    Article  Google Scholar 

  12. Awh, E., Armstrong, K.M. & Moore, T. Visual and oculomotor selection: links, causes and implications for spatial attention. Trends Cogn. Sci. 10, 124–130 (2006).

    Article  Google Scholar 

  13. Cavanagh, P., Hunt, A.R., Afraz, A. & Rolfs, M. Visual stability based on remapping of attention pointers. Trends Cogn. Sci. 14, 147–153 (2010).

    Article  Google Scholar 

  14. 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).

    Article  CAS  Google Scholar 

  15. Sommer, M.A. & Wurtz, R.H. Influence of the thalamus on spatial visual processing in frontal cortex. Nature 444, 374–377 (2006).

    Article  CAS  Google Scholar 

  16. Gottlieb, J.P., Kusunoki, M. & Goldberg, M.E. The representation of visual salience in monkey parietal cortex. Nature 391, 481–484 (1998).

    Article  CAS  Google Scholar 

  17. Berman, R. & Colby, C.L. Attention and active vision. Vision Res. 49, 1233–1248 (2009).

    Article  Google Scholar 

  18. Mathôt, S. & Theeuwes, J. Evidence for the predictive remapping of visual attention. Exp. Brain Res. 200, 117–122 (2010).

    Article  Google Scholar 

  19. Melcher, D. Predictive remapping of visual features precedes saccadic eye movements. Nat. Neurosci. 10, 903–907 (2007).

    Article  CAS  Google Scholar 

  20. Becker, W. & Jürgens, R. An analysis of the saccadic system by means of double step stimuli. Vision Res. 19, 967–983 (1979).

    Article  CAS  Google Scholar 

  21. Hallett, P.E. & Lightstone, A.D. Saccadic eye movements to flashed targets. Vision Res. 16, 107–114 (1976).

    Article  CAS  Google Scholar 

  22. Collins, T., Rolfs, M., Deubel, H. & Cavanagh, P. Post-saccadic location judgments reveal remapping of saccade targets to non-foveal locations. J. Vis. 9, 1–9 (2009).

    Article  Google Scholar 

  23. Karni, A. & Sagi, D. Where practice makes perfect in texture discrimination: evidence for primary visual-cortex plasticity. Proc. Natl. Acad. Sci. USA 88, 4966–4970 (1991).

    Article  CAS  Google Scholar 

  24. Polat, U. & Sagi, D. Lateral interactions between spatial channels: suppression and facilitation revealed by lateral masking experiments. Vision Res. 33, 993–999 (1993).

    Article  CAS  Google Scholar 

  25. Solomon, J.A. The effect of spatial cues on visual sensitivity. Vision Res. 44, 1209–1216 (2004).

    Article  Google Scholar 

  26. Melcher, D. & Colby, C.L. Trans-saccadic perception. Trends Cogn. Sci. 12, 466–473 (2008).

    Article  Google Scholar 

  27. Knapen, T., Rolfs, M., Wexler, M. & Cavanagh, P. The reference frame of the tilt aftereffect. J. Vis. 10, 1–13 (2010).

    Article  Google Scholar 

  28. Guthrie, B.L., Porter, J.D. & Sparks, D.L. Corollary discharge provides accurate eye position information to the oculomotor system. Science 221, 1193–1195 (1983).

    Article  CAS  Google Scholar 

  29. Sommer, M.A. & Wurtz, R.H. A pathway in primate brain for internal monitoring of movements. Science 296, 1480–1482 (2002).

    Article  CAS  Google Scholar 

  30. Chen, Y. et al. Task difficulty modulates the activity of specific neuronal populations in primary visual cortex. Nat. Neurosci. 11, 974–982 (2008).

    Article  CAS  Google Scholar 

  31. Macknik, S.L. & Martinez-Conde, S. Chapter 81: The role of feedback in visual attention and awareness. in The Cognitive Neurosciences 4th edn. (ed. Gazzaniga, M.S.) 1165–1179 (MIT Press, Cambridge, Massachusetts, 2009).

  32. Golomb, J.D., Chun, M.M. & Mazer, J.A. The native coordinate system of spatial attention is retinotopic. J. Neurosci. 28, 10654–10662 (2008).

    Article  CAS  Google Scholar 

  33. Brainard, D.H. The Psychophysics Toolbox. Spat. Vis. 10, 433–436 (1997).

    Article  CAS  Google Scholar 

  34. Pelli, D.G. The VideoToolbox software for visual psychophysics: transforming numbers into movies. Spat. Vis. 10, 437–442 (1997).

    Article  CAS  Google Scholar 

  35. Cornelissen, F.W., Peters, E.M. & Palmer, J. The Eyelink Toolbox: eye tracking with MATLAB and the Psychophysics Toolbox. Behav. Res. Methods Instrum. Comput. 34, 613–617 (2002).

    Article  Google Scholar 

  36. Watson, A.B. & Pelli, D.G. QUEST: a Bayesian adaptive psychometric method. Percept. Psychophys. 33, 113–120 (1983).

    Article  CAS  Google Scholar 

  37. Engbert, R. & Mergenthaler, K. Microsaccades are triggered by low retinal image slip. Proc. Natl. Acad. Sci. USA 103, 7192–7197 (2006).

    Article  CAS  Google Scholar 

  38. Rolfs, M., Engbert, R. & Kliegl, R. Crossmodal coupling of oculomotor control and spatial attention in vision and audition. Exp. Brain Res. 166, 427–439 (2005).

    Article  Google Scholar 

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Acknowledgements

We thank C. Buß for help with data acquisition. This work was supported by the 7th Framework Program of the European Commission (Marie Curie International Outgoing Fellowship 235625 awarded to M.R.), by Deutsche Forschungsgemeinschaft (GRK 1091, as a fellowship to D.J.) and by a Chaire d'Excellence grant to P.C.

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Authors

Contributions

M.R., D.J., H.D. and P.C. designed the experiments. M.R. and D.J. conducted the experiments and analyzed the data. M.R. and P.C. wrote the manuscript. P.C. and H.D. supervised the project. All of the authors discussed the results and commented on the manuscript.

Corresponding authors

Correspondence to Martin Rolfs or Patrick Cavanagh.

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The authors declare no competing financial interests.

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Rolfs, M., Jonikaitis, D., Deubel, H. et al. Predictive remapping of attention across eye movements. Nat Neurosci 14, 252–256 (2011). https://doi.org/10.1038/nn.2711

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