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The detection of visual signals by macaque frontal eye field during masking

Abstract

The neural link between a sensory signal and its behavioral report was investigated in macaques trained to locate an intermittently detectable visual target. Neurons in the frontal eye field, an area involved in converting the outcome of visual processing into motor commands, responded at short latencies to the target stimulus whether or not the monkey reported its presence. Neural activity immediately preceding the visual response to the mask was significantly greater on hits than on misses, and was significantly greater on false alarms than on correct rejections. The results show that visual signals masked by light are not filtered out at early stages of visual processing; furthermore, the magnitude of early visual responses in prefrontal cortex predicts the behavioral report.

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Figure 1: Backward masking task and behavioral performance.
Figure 2: Responses of a visual neuron in the frontal eye field during the backward-masking task.
Figure 3: Contrast of responses for different conditions.
Figure 4: Frequency of normalized firing rates for 45 FEF neurons.

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References

  1. Logothetis, N. K. & Schall, J. D. Neuronal correlates of subjective visual perception. Science 245, 761–763 (1989).

    Article  CAS  Google Scholar 

  2. Leopold, D. A. & Logothetis, N. K. Activity changes in early visual cortex reflect monkeys' percepts during binocular rivalry. Nature 379, 549–553 ( 1996).

    Article  CAS  Google Scholar 

  3. Sheinberg, D. L. & Logothetis, N. K. The role of temporal cortical areas in perceptual organization. Proc. Natl. Acad. Sci. USA 94, 3408–3413 (1997).

    Article  CAS  Google Scholar 

  4. Britten, K. H., Newsome, W. T., Shadlen, M. N., Celebrini, S. & Movshon, J. A. A relationship between behavioral choice and the visual responses of neurons in macaque MT. Vis. Neurosci. 13, 87–100 ( 1996).

    Article  CAS  Google Scholar 

  5. Schall, J. D., Morel, A., King, D. J. & Bullier, J. Topography of visual cortex connections with frontal eye field in macaque: Convergence and segregation of processing streams. J. Neurosci. 15, 4464–4487 (1995).

    Article  CAS  Google Scholar 

  6. Schall, J. D. (1997) in Cerebral Cortex (vol. 12): Extrastriate Cortex of Primates (eds. Rockland, K. S., Peters, A. & Kaas, J. H.) 527–638 (Plenum, New York, 1997).

    Google Scholar 

  7. Crick, F. & Koch, C. Are we aware of neural activity in primary visual cortex? Nature 375, 121– 123 (1995).

    Article  CAS  Google Scholar 

  8. Koch, C. & Braun, J. Towards the neuronal correlate of visual awareness. Curr. Opin. Neurobiol. 6, 158–164 (1996).

    Article  CAS  Google Scholar 

  9. Breitmeyer, B. G. Visual Masking: An Integrative Approach (Oxford Univ. Press, New York, 1984).

    Google Scholar 

  10. Green, D. M. & Swets, J. A. Signal Detection Theory and Psychophysics (Wiley, New York, 1966).

    Google Scholar 

  11. 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 

  12. Schiller, P. H. Single unit analysis of backward visual masking and metacontrast in the cat lateral geniculate nucleus. Vision Res. 8, 855–866 (1968).

    Article  CAS  Google Scholar 

  13. Fehmi, L. G., Adkins, J. W. & Lindsley, D. B. Electrophysiological correlates of visual perceptual masking in monkeys. Exp. Brain Res. 7, 299 –316 (1969).

    Article  CAS  Google Scholar 

  14. Coenen, A. M. L. & Eijkman, E. G. J. Cat optic tract and geniculate unit responses corresponding to human visual masking effects. Exp. Brain Res. 15, 441– 451 (1972).

    CAS  PubMed  Google Scholar 

  15. Judge, S. J., Wurtz, R. H. & Richmond, B.J. Vision during saccadic eye movements. I. Visual interactions in striate cortex. J. Neurophysiol. 43, 1133–1155 (1980).

    Article  CAS  Google Scholar 

  16. Rolls, E. T. & Tovee, M. J. Processing speed in the cerebral cortex and the neurophysiology of visual masking. Proc. R. Soc. Lond. B Biol. Sci. 257, 9–15 (1994).

    Article  CAS  Google Scholar 

  17. Kovács, G., Vogels, R. & Orban, G. A. Cortical correlate of pattern backward masking. Proc. Natl. Acad. Sci. USA 92, 5587– 5591 (1995).

    Article  Google Scholar 

  18. Macknick, S. L. & Livingstone, M. S. Neuronal correlates of visibility and invisibility in the primate visual system. Nat. Neurosci. 1, 144–149 (1998).

    Article  Google Scholar 

  19. Maunsell, J. H. R. The brain's visual world: representation of visual targets in cerebral cortex. Science 270, 764–769 (1995).

    Article  CAS  Google Scholar 

  20. Luck, S. J., Chelazzi, L., Hillyard, S. A. & Desimone, R. Neural mechanisms of spatial selective attention in areas V1, V2, and V4 of macaque visual cortex. J. Neurophysiol. 77, 24–42 (1997).

    Article  CAS  Google Scholar 

  21. Sakagami, M. & Niki, H. Encoding of behavioral significance of visual stimuli by primate prefrontal neurons: relation to relevant task conditions. Exp. Brain Res. 97, 423– 436 (1994).

    Article  CAS  Google Scholar 

  22. Watanabe, M. Reward expectancy in primate prefrontal neurons. Nature 382, 629–632 (1996).

    Article  CAS  Google Scholar 

  23. Rainer, G., Asaad, W. F. & Miller, E. K. Selective representation of relevant information by neurons in the primate prefrontal cortex. Nature 393, 577–579 (1998).

    Article  CAS  Google Scholar 

  24. Nowak, L. & Bullier, J. in Cerebral Cortex (vol. 12): Extrastriate Cortex of Primates (eds. Rockland, K. S., Peters, A. & Kaas, J. H.) 205–241 (Plenum, New York, 1997).

    Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  27. Wurtz, R. H. & Mohler, C. W. Enhancement of visual responses in monkey striate cortex and frontal eye fields. J. Neurophysiol. 39, 766–772 ( 1976).

    Article  CAS  Google Scholar 

  28. Goldberg, M. E. & Bushnell, M. C. Behavioral enhancement of visual responses in monkey cerebral cortex. II. Modulation in frontal eye fields specifically related to saccades. J. Neurophysiol. 46, 773–787 ( 1981).

    Article  CAS  Google Scholar 

  29. Arieli, A., Sterkin, A., Grinvald, A. & Aertsen, A. Dynamics of ongoing activity: explanation of the large variability in evoked cortical responses. Science 273, 1868– 1871 (1996).

    Article  CAS  Google Scholar 

  30. Schall, J. D., Hanes, D. P., Thompson, K. G. & King, D. J. Saccade target selection in frontal eye field of macaque. I. Visual and premovement activation. J. Neurosci. 15, 6905– 6918 (1995).

    Article  CAS  Google Scholar 

  31. Hanes, D. P., Thompson, K. G. & Schall, J. D. Relationship of presaccadic activity in frontal eye field and supplementary eye field to saccade initiation in macaque: Poisson spike train analysis. Exp. Brain Res. 103, 85–96 (1995).

    Article  CAS  Google Scholar 

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Acknowledgements

This work was supported by R01-EY08890, P30-EY08126, the McDonnell-Pew Program in Cognitive Neuroscience and the McKnight Endowment Fund for Neuroscience. We thank N. Bichot, R. Blake, R. Fox, J. Lappin, and M. Shadlen for discussions about this work. J. S. is a Kennedy Center Investigator.

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Correspondence to Kirk G. Thompson.

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Thompson, K., Schall, J. The detection of visual signals by macaque frontal eye field during masking . Nat Neurosci 2, 283–288 (1999). https://doi.org/10.1038/6398

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