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Neuronal switching of sensorimotor transformations for antisaccades

Abstract

The influence of cognitive context on orienting behaviour can be explored using the mixed memory-prosaccade, memory-antisaccade task. A symbolic cue, such as the colour of a visual stimulus, instructs the subject to make a brief, rapid eye movement (a saccade) either towards the stimulus (prosaccade) or in the opposite direction (antisaccade)1,2,3. Thus, the appropriate sensorimotor transformation must be switched on to execute the instructed task. Despite advances in our understanding of the neuronal processing of antisaccades4,5,6,7,8, it remains unclear how the brain selects and computes the sensorimotor transformation leading to an antisaccade. Here we show that area LIP of the posterior parietal cortex is involved in these processes. LIP's population activity turns from the visual direction to the motor direction during memory-antisaccade trials. About one-third of the visual neurons in LIP produce a brisk, transient discharge in certain memory-antisaccade trials. We call this discharge ‘paradoxical’ because its timing is visual-like but its direction is motor. The paradoxical discharge shows, first, that switching occurs already at the level of visual cells, as previously proposed by Schlag-Rey and colleagues5; and second, that this switching is accomplished very rapidly, within 50 ms from the arrival of the visual signals in LIP.

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Figure 1: Cartoons of involved operations, hypotheses and task details.
Figure 2: Responses of single PPC neurons.
Figure 3: Mean differential activity for all 400 units studied. (Summed DA divided by number of units.) The DA is plotted in black.
Figure 4: Illustration of the paradoxical activity.

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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. Amador, N., Schlag-Rey, M. & Schlag, J. Primate antisaccades. I. Behavioral characteristics. J. Neurophysiol. 80, 1775–1786 (1998).

    Article  CAS  Google Scholar 

  3. Everling, S. & Fischer, B. The antisaccade: a review of basic research and clinical studies. Neuropsychologia 36, 885–899 (1998).

    Article  CAS  Google Scholar 

  4. 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 

  5. Schlag-Rey, M., Amador, N., Sanchez, H. & Schlag, J. Antisaccade performance predicted by neuronal activity in the supplementary eye field. Nature 390, 398–401 (1997).

    Article  ADS  CAS  Google Scholar 

  6. Gottlieb, J. & Goldberg, M. E. Activity of neurons in the lateral intraparietal area of the monkey during an antisaccade task. Nature Neurosci. 2, 906–912 (1999).

    Article  CAS  Google Scholar 

  7. Everling, S., Dorris, M. C., Klein, R. M. & Munoz, D. P. Role of primate superior colliculus in preparation and execution of anti-saccades and pro-saccades. J. Neurosci. 19, 2740–2754 (1999).

    Article  CAS  Google Scholar 

  8. Everling, S. & Munoz, D. P. Neuronal correlates for preparatory set associated with pro-saccades and anti-saccades in the primate frontal eye field. J. Neurosci. 20, 387–400 (2000).

    Article  CAS  Google Scholar 

  9. Hikosaka, O. & Wurtz, R. H. Visual and oculomotor functions of monkey substantia nigra pars reticulata. III. Memory-contingent visual and saccade responses. J. Neurophysiol. 49, 1268–1284 (1983).

    Article  CAS  Google Scholar 

  10. Gnadt, J. W. & Andersen, R. A. Memory related motor planning activity in posterior parietal cortex of macaque. Exp. Brain Res. 70, 216–220 (1988).

    CAS  Google Scholar 

  11. Barash, S., Bracewell, R. M., Fogassi, L., Gnadt, J. W. & Andersen, R. A. Saccade-related activity in the lateral intraparietal area. II. Spatial properties. J. Neurophysiol. 66, 1109–1124 (1991).

    Article  CAS  Google Scholar 

  12. Barash, S., Bracewell, R. M., Fogassi, L., Gnadt, J. W. & Andersen, R. A. Saccade-related activity in the lateral intraparietal area. I. Temporal properties; comparison with area 7a. J. Neurophysiol. 66, 1095–1108 (1991).

    Article  CAS  Google Scholar 

  13. 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 

  14. Snyder, L. H., Batista, A. P. & Andersen, R. A. Coding of intention in the posterior parietal cortex. Nature 386, 167–170 (1997).

    Article  ADS  CAS  Google Scholar 

  15. Chafee, M. V. & Goldman-Rakic, P. S. Matching patterns of activity in primate prefrontal area 8a and parietal area 7ip neurons during a spatial working memory task. J. Neurophysiol. 79, 2919–2940 (1998).

    Article  CAS  Google Scholar 

  16. 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 

  17. Andersen, R. A. in Handbook of Physiology, Section 1: The Nervous System (eds Mountcastle, V. B., Plum, F. & Geiger, S. R.) 483–518 (Am. Physiol. Soc., Bethesda, 1987).

    Google Scholar 

  18. Everling, S., Spantekow, A., Krappmann, P. & Flohr, H. Event-related potentials associated with correct and incorrect responses in a cued antisaccade task. Exp. Brain Res. 118, 27–34 (1998).

    Article  CAS  Google Scholar 

  19. Horwitz, G. D. & Newsome, W. T. Separate signals for target selection and movement specification in the superior colliculus. Science 284, 1158–1161 (1999).

    Article  ADS  CAS  Google Scholar 

  20. Grunewald, A., Linden, J. F. & Andersen, R. A. Responses to auditory stimuli in macaque lateral intraparietal area. I. Effects of training. J. Neurophysiol. 82, 330–342 (1999).

    Article  CAS  Google Scholar 

  21. Thier, P. & Andersen, R. A. Electrical microstimulation distinguishes distinct saccade-related areas in the posterior parietal cortex. J. Neurophysiol. 80, 1713–1735 (1998).

    Article  CAS  Google Scholar 

  22. Colby, C. L., Gattass, R., Olson, C. R. & Gross, C. G. Topographical organization of cortical afferents to extrastriate visual area PO in the macaque: a dual tracer study. J. Comp. Neurol. 269, 392–413 (1988).

    Article  CAS  Google Scholar 

  23. Barash, S., Melikyan, A., Sivakov, A. & Tauber, M. Shift of visual fixation dependent on background illumination. J. Neurophysiol. 79, 2766–2781 (1998).

    Article  CAS  Google Scholar 

  24. Newsome, W. T., Britten, K. H. & Movshon, J. A. Neuronal correlates of a perceptual decision. Nature 341, 52–54 (1989).

    Article  ADS  CAS  Google Scholar 

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Acknowledgements

We thank E. Ahissar for his involvement, and A. Melikyan and X. Wang for participation in some experiments. We thank M. Glickstein, P. Thier, E. Seidemann, Y. Ritov and M. Tsodyks for discussions and for reading the manuscript. This work was supported by the Israel Science Foundation, and by the Murray H. and Meyer Grodetsky Center for Research of Higher Brain Functions and the Einhorn-Dominic Institute of Brain Research at the Weizmann Institute, and by the Paul Godfrey Research Foundation.

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Correspondence to Shabtai Barash.

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Zhang, M., Barash, S. Neuronal switching of sensorimotor transformations for antisaccades. Nature 408, 971–975 (2000). https://doi.org/10.1038/35050097

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