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Antisaccade performance predicted by neuronal activity in the supplementary eye field

Nature volume 390, pages 398–401 (1997)Cite this article

Abstract

The voluntary control of gaze implies the ability to make saccadic eye movements specified by abstract instructions, as well as the ability to repress unwanted orientating to sudden stimuli. Both of these abilities are challenged in the antisaccade task, because it requires subjects to look at an unmarked location opposite to a flashed stimulus, without glancing at it1,2. Performance on this task depends on the frontal/prefrontal cortex and related structures3,4,5,6,7,8, but the neuronal operations underlying antisaccades are not understood. It is not known, for example, how excited visual neurons that normally trigger a saccade to a target (a prosaccade) can activate oculomotor neurons directing gaze in the opposite direction. Visual neurons might, perhaps, alter their receptive fields depending on whether they receive a pro- or antisaccade instruction. If the receptive field is not altered, the antisaccade goal must be computed and imposed from the top down to the appropriate oculomotor neurons. Here we show, using recordings from the supplementary eye field (a frontal cortex oculomotor centre) in monkeys, that visual and movement neurons retain the same spatial selectivity across randomly mixed pro- and antisaccade trials. However, these neurons consistently fire more before antisaccades than prosaccades with the same trajectories, suggesting a mechanism through which voluntary antisaccade commands can override reflexive glances.

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Figure 1: Spatial display and sequence of stimuli and saccades.
Figure 2: Performance of delayed saccades and activity profiles of pro- and antisaccades.
Figure 3: Performance of non-delayed saccades and activity profiles of pro- and antisaccades.
Figure 4: Activity of antisaccades and prosaccades in movement cells and visual cells.

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References

  1. Hallett, P. E. Primary and secondary saccades to goals defined by instructions. Vision Res. 18, 1279–1296 (1978).

    Article  CAS  Google Scholar 

  2. Fischer, B. & Weber, H. Characteristics of “anti” saccades in man. Exp. Brain Res. 89, 415–424 (1992).

    Article  CAS  Google Scholar 

  3. Guitton, D., Buchtel, H. A. & Douglas, R. M. Frontal lobe lesions in man cause difficulties in suppressing reflexive glances and in generating goal-directed saccades. Exp. Brain Res. 58, 455–472 (1985).

    Article  CAS  Google Scholar 

  4. Pierrot-Deseilligny, C. H., Rivaud, S., Gaymard, B. & Agid, Y. Cortical control of reflexive visually-guided saccades. Brain 114, 1473–1485 (1991).

    Article  Google Scholar 

  5. O'Driscoll, G. A. et al . Functional neuroanatomy of antisaccade eye movements investigated with positron emission tomography. Proc. Natl Acad. Sci. USA 92, 925–929 (1995).

    Article  ADS  CAS  Google Scholar 

  6. Sweeney, J. A. et al . Positron emission tomography study of voluntary saccadic eye movements and spatial working memory. J. Neurophysiol. 75, 454–468 (1996).

    Article  CAS  Google Scholar 

  7. Tian, J. R., Zee, D. S., Lasker, A. G. & Folstein, S. E. Saccades in Huntington's disease: predictive tracking and interaction between release of fixation and initiation of saccades. Neurology 41, 875–881 (1991).

    Article  CAS  Google Scholar 

  8. Funahashi, S., Chafee, M. V. & Goldman-Rakic, P. S. Prefrontal neuronal activity in Rhesus monkeys performing a delayed anti-saccade task. Nature 365, 753–756 (1993).

    Article  ADS  CAS  Google Scholar 

  9. Remington, R. W., Johnston, J. C. & Yantis, S. Involuntary attentional capture by abrupt onsets. Percept. Psychophys. 51, 279–290 (1992).

    Article  CAS  Google Scholar 

  10. 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  ADS  CAS  Google Scholar 

  11. Salzman, C. D. & Newsome, W. T. Neural mechanisms for forming a perceptual decision. Science 264, 231–237 (1994).

    Article  ADS  CAS  Google Scholar 

  12. Schlag-Rey, M., Schlag, J. & Sanchez, H. FEF neuronal activity during monkey performance of antisaccade tasks. Soc. Neurosci. Abstr. 19, 785 (1993).

    Google Scholar 

  13. 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 

  14. Schlag, J. & Schlag-Rey, M. Evidence for a supplementary eye field. J. Neurophysiol. 57, 179–200 (1987).

    Article  CAS  Google Scholar 

  15. Schall, J. D. Neuronal activity related to visually guided saccadic eye movements in the supplementary motor area of Rhesus monkeys. J. Neurophysiol. 66, 530–558 (1991).

    Article  CAS  Google Scholar 

  16. Shook, B. L., Schlag-Rey, M. & Schlag, J. Primate supplementary eye field: I. Comparative aspects of mesencephalic and pontine connections. J. Comp. Neurol. 301, 618–642 (1990).

    Article  CAS  Google Scholar 

  17. Chen, L. L. & Wise, S. P. Evolution of directional preferences in the supplementary eye field during acquisition of conditional oculomotor associations. J. Neurosci. 16, 3067–3081 (1996).

    Article  CAS  Google Scholar 

  18. Rugg, M. D. & Coles, M. G. H. Electrophysiology of Mind: Event-Related Brain Potentials and Cognition(Oxford Univ. Press, (1995)).

    Google Scholar 

  19. Schlag, J. & Schlag-Rey, M. Supplementary eye field: influence of eye position on neural signals of fixation. Exp. Brain Res. 90, 302–306 (1992).

    Article  CAS  Google Scholar 

  20. Weber, H. Presaccadic processes in the generation of pro and anti saccades in human subjects: A reaction-time study. Perception 24, 1265–1280 (1995).

    Article  CAS  Google Scholar 

  21. Goldberg, M. E. & Segraves, M. A. in The Neurobiology of Saccadic Eye Movements(eds Wurtz, R. H. & Goldberg, M. E.) 283–313 (Elsevier, New York, (1989)).

    Google Scholar 

  22. Segraves, M. A. & Park, K. The relationship of monkey frontal eye field activity to saccade dynamics. J. Neurophysiol. 69, 1880–1889 (1993).

    Article  CAS  Google Scholar 

  23. Hanes, D. P. & Schall, J. D. Neural control of voluntary movement initiation. Science 274, 427–430 (1996).

    Article  ADS  CAS  Google Scholar 

  24. Thompson, K. G., Hanes, D. P., Bichot, N. P. & Schall, J. D. Perceptual and motor processing stages identified in the activity of macaque frontal eye field neurons during visual search. J. Neurophysiol. 76, 4040–4055 (1996).

    Article  CAS  Google Scholar 

  25. Schlag, J., Dassonville, P. & Schlag-Rey, M. Functional interaction of the two frontal eye fields prior to saccade in monkey. J. Neurophysiol.(in the press).

  26. Schlag-Rey, M., Schlag, J. & Dassonville, P. How the frontal eye field can impose a saccade goal on superior colliculus neurons. J. Neurophysiol. 67, 1003–1005 (1992).

    Article  CAS  Google Scholar 

  27. Schiller, P. H., Sandell, J. H. & Maunsell, J. H. R. Effect of frontal eye field and superior colliculus lesions on saccadic latencies in the Rhesus monkey. J. Neurophysiol. 57, 1033–1049 (1987).

    Article  CAS  Google Scholar 

  28. Passingham, R. E. The Frontal Lobes and Voluntary Action(Oxford Univ. Press, (1993)).

    Google Scholar 

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

    Article  CAS  Google Scholar 

  30. Russo, G. S. & Bruce, C. J. Neurons in the supplementary eye field of Rhesus monkeys code visual targets and saccadic eye movements in an oculocentric coordinate system. J. Neurophysiol. 76, 825–848 (1996).

    Article  CAS  Google Scholar 

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Acknowledgements

We thank P. Dassonville, A. Pouget and J.-R. Tian for comments and suggestions, and the National Eye Institute for financial support.

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Authors and Affiliations

  1. Department of Neurobiology and Brain Research Institute, UCLA School of Medicine, Los Angeles, 90095-1763, California, USA

    Madeleine Schlag-Rey, Nelly Amador, Henry Sanchez & John Schlag

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  1. Madeleine Schlag-Rey
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  2. Nelly Amador
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  3. Henry Sanchez
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  4. John Schlag
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Correspondence to Madeleine Schlag-Rey.

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Schlag-Rey, M., Amador, N., Sanchez, H. et al. Antisaccade performance predicted by neuronal activity in the supplementary eye field. Nature 390, 398–401 (1997). https://doi.org/10.1038/37114

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