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Spatiotopic temporal integration of visual motion across saccadic eye movements

Abstract

Saccadic eye movements pose many challenges for stable and continuous vision, such as how information from successive fixations is amalgamated into a single precept. Here we show in humans that motion signals are temporally integrated across separate fixations, but only when the motion stimulus falls either on the same retinal region (retinotopic integration) or on different retinal positions that correspond to the same external spatial coordinates (spatiotopic integration). We used individual motion signals that were below detection threshold, implicating spatiotopic trans-saccadic integration in relatively early stages of visual processing such as the middle temporal area (MT) or V5 of visual cortex. The trans-saccadic buildup of important congruent visual information while irrelevant non-congruent information fades could provide a simple and robust strategy to stabilize perception during eye movements.

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Figure 1: Schematic representation of the visual stimuli for experiment 1 (a) and experiment 2 (b), and relative time course of the events (c).
Figure 2: Motion coherence sensitivity as a function of temporal delay between the two motion signals.
Figure 3: Percentage correct motion discrimination as a function of motion strength in two subjects (MCM, top row, and DM, bottom row) for retinotopic integration across saccades (see Fig. 1b,c).
Figure 4: Accuracy of motion discrimination as a function of motion strength for control conditions for DM (top) and AB (bottom).

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References

  1. Land, M.F. & Nilsson, D.E. Animal Eyes (Oxford Univ. Press, Oxford, 2001).

    Google Scholar 

  2. Jonides, J., Irwin, D. & Yantis, S. Failure to integration visual information from successive fixations. Science 222, 188 (1983).

    Article  CAS  Google Scholar 

  3. Bridgeman, B. & Mayer, M. Failure to integrate visual information from successive fixations. Bull. Psychonomic Soc. 21, 285–286 (1983).

    Article  Google Scholar 

  4. Irwin, D.E. Information integration across saccadic eye movements. Cognit. Psychol. 23, 420–456 (1991).

    Article  CAS  Google Scholar 

  5. Hayhoe, M., Lachter, J. & Feldman, J. Integration of form across saccadic eye movements. Perception 20, 393–402 (1991).

    Article  CAS  Google Scholar 

  6. Barlow, H.B. Temporal and spatial summation in human vision at different background intensities. J. Physiol. (Lond.) 141, 337–350 (1958).

    Article  CAS  Google Scholar 

  7. Burr, D.C. & Santoro, L. Temporal integration of optic flow, measured by contrast and coherence thresholds. Vision Res. 41, 1891–1899 (2001).

    Article  CAS  Google Scholar 

  8. Graziano, M.S., Yap, G.S. & Gross, C.G. Coding of visual space by premotor neurons. Science 266, 1054–1057 (1994).

    Article  CAS  Google Scholar 

  9. Snyder, L.H., Grieve, K.L., Brotchie, P. & Andersen, R.A. Separate body- and world-referenced representations of visual space in parietal cortex. Nature 394, 887–891 (1998).

    Article  CAS  Google Scholar 

  10. Duhamel, J., Bremmer, F., BenHamed, S. & Graf, W. Spatial invariance of visual receptive fields in parietal cortex neurons. Nature 389, 845–848 (1997).

    Article  CAS  Google Scholar 

  11. Galletti, C., Battaglini, P.P. & Fattori, P. Parietal neurons encoding spatial locations in craniotopic coordinates. Exp. Brain Res. 96, 221–229 (1993).

    Article  CAS  Google Scholar 

  12. Deubel, H. & Schneider, W.X. Saccade target selection and object recognition: evidence for a common attentional mechanism. Vision Res. 36, 1827–1837 (1996).

    Article  CAS  Google Scholar 

  13. Burr, D.C., Holt, J., Johnstone, J.R. & Ross, J. Selective depression of motion sensitivity during saccades. J. Physiol. (Lond.) 333, 1–15 (1982).

    Article  CAS  Google Scholar 

  14. Shiori, S. & Cavanagh, P. Saccadic suppression of low-level motion. Vision Res. 29, 915–928 (1989).

    Article  Google Scholar 

  15. Saenz, M., Buracas, G.T. & Boynton, G.M. Global effects of feature-based attention in human visual cortex. Nat. Neurosci. 5, 631–632 (2002).

    Article  CAS  Google Scholar 

  16. Wexler, M., Panerai, F., Lamouret, I. & Droulez, J. Self-motion and the perception of stationary objects. Nature 409, 85–88 (2001).

    Article  CAS  Google Scholar 

  17. Melcher, D. Persistence of visual memory for scenes. Nature 412, 401 (2001).

    Article  CAS  Google Scholar 

  18. Brockmole, J.R., Wang, R.F. & Irwin, D.E. Temporal integration between visual images and visual percepts. J. Exp. Psychol. Hum. Percept. Perform. 28, 315–334 (2002).

    Article  Google Scholar 

  19. 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  Google Scholar 

  20. Burr, D.C., Morrone, M.C. & Vaina, L.M. Large receptive fields for optic flow in humans. Vision Res. 38, 1731–1743 (1998).

    Article  CAS  Google Scholar 

  21. 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 

  22. Colby, C.L., Duhamel, J.R. & Goldberg, M.E. Visual, presaccadic, and cognitive activation of single neurons in monkey lateral intraparietal area. J. Neurophysiol. 76, 2841–2852 (1996).

    Article  CAS  Google Scholar 

  23. Nakamura, K. & Colby, C.L. Updating of the visual representation in monkey striate and extrastriate cortex during saccades. Proc. Natl. Acad. Sci. USA 99, 4026–4031 (2002).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  25. Salzman, C.D., Britten, K.H. & Newsome, W.T. Cortical microstimulation influences perceptual judgments of motion direction. Nature 346, 106 (1990).

    Article  Google Scholar 

  26. Rees, G., Friston, K. & Koch, C. A direct quantitative relationship between the functional properties of human and macaque V5. Nat. Neurosci. 3, 716–723 (2000).

    Article  CAS  Google Scholar 

  27. Bremmer, F., Ilg, U.J., Thiele, A., Distler, C. & Hoffman, K.P. Eye position effects in monkey cortex. I. Visual and pursuit-related activity in extrastriate areas MT and MST. J. Neurophysiol. 77, 944–961 (1997).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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Acknowledgements

This research was supported by Human Frontiers Science Program and Miur Cofin 2001. Special thanks to D. Burr for helpful discussion and criticisms of the manuscript.

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Correspondence to M Concetta Morrone.

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Melcher, D., Morrone, M. Spatiotopic temporal integration of visual motion across saccadic eye movements. Nat Neurosci 6, 877–881 (2003). https://doi.org/10.1038/nn1098

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