Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Filtering of neural signals by focused attention in the monkey prefrontal cortex

Abstract

Prefrontal cortex is thought to be important in attention and awareness. Here we recorded the activity of prefrontal neurons in monkeys carrying out a focused attention task. Having directed attention to one location, monkeys monitored a stream of visual objects, awaiting a predefined target. Although neurons rarely discriminated between one non-target and another, they commonly discriminated between targets and non-targets. From the onset of the visual response, this target/non-target discrimination was effectively eliminated when the same objects appeared at an unattended location in the opposite visual hemifield. The results show that, in prefrontal cortex, filtering of ignored locations is strong, early and spatially global. Such filtering may be important in blindness to unattended signals—a conspicuous aspect of human selective attention.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Figure 1: The focused attention task and recording locations.
Figure 2: Unilateral condition; activity of prefrontal cortex (PFC) neurons that showed object (target versus non-target) selectivity.
Figure 3: Neural activity for selected stimulus-response combinations.
Figure 4: Bilateral condition; activity in the selected cell sample for the different stimulus combinations of target and non-target objects.
Figure 5: Influence of attention on object selectivity at the preferred location.

Similar content being viewed by others

References

  1. Rock, I., Linnett, C.M., Grant, P. & Mack, A. Perception without attention: results of a new method. Cogn. Psychol. 24, 502–534 (1992).

    Article  CAS  PubMed  Google Scholar 

  2. Broadbent, D.E. Perception and Communication (Pergamon, London, 1958).

    Book  Google Scholar 

  3. Desimone, R. & Duncan, J. Neural mechanisms of selective visual attention. Annu. Rev. Neurosci. 18, 193–222 (1995).

    Article  CAS  PubMed  Google Scholar 

  4. Miller, E.K. & Cohen, J.D. An integrative theory of prefrontal cortex function. Annu. Rev. Neurosci. 24, 167–202 (2001).

    Article  CAS  PubMed  Google Scholar 

  5. Duncan, J. An adaptive coding model of neural function in prefrontal cortex. Nat. Rev. Neurosci. 2, 820–829 (2001).

    Article  CAS  PubMed  Google Scholar 

  6. 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  PubMed  Google Scholar 

  7. 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  PubMed  PubMed Central  Google Scholar 

  8. Hasegawa, R.P., Matsumoto, M. & Mikami, A. Search target selection in monkey prefrontal cortex. J. Neurophysiol. 84, 1692–1696 (2000).

    Article  CAS  PubMed  Google Scholar 

  9. Lumer, E.D., Friston, K.J. & Rees, G. Neural correlates of perceptual rivalry in the human brain. Science 280, 1930–1934 (1998).

    Article  CAS  PubMed  Google Scholar 

  10. Beck, D.M., Rees, G., Frith, C.D. & Lavie, N. Neural correlates of change detection and change blindness. Nat. Neurosci. 4, 645–650 (2001).

    Article  CAS  PubMed  Google Scholar 

  11. Dehaene, S. et al. Cerebral mechanisms of word masking and unconscious repetition priming. Nat. Neurosci. 4, 752–758 (2001).

    Article  CAS  PubMed  Google Scholar 

  12. Posner, M.I., Snyder, C.R.R. & Davidson, B.J. Attention and the detection of signals. J. Exp. Psychol. 109, 160–174 (1980).

    Article  CAS  PubMed  Google Scholar 

  13. Van Voorhis, S. & Hillyard, S.A. Visual evoked potentials and selective attention to points in space. Percept. Psychophys. 22, 54–62 (1977).

    Article  Google Scholar 

  14. Corbetta, M., Miezin, F.M., Shulman, G.L. & Petersen, S.E. A PET study of visuospatial attention. J. Neurosci. 13, 1202–1226 (1993).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Rainer, G., Asaad, W.F. & Miller, E.K. Memory fields of neurons in the primate prefrontal cortex. Proc. Natl. Acad. Sci. USA 95, 15008–15013 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. 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  PubMed  Google Scholar 

  17. Funahashi, S., Bruce, C.J. & Goldman-Rakic, P.S. Mnemonic coding of visual space in the monkey's dorsolateral prefrontal cortex. J. Neurophysiol. 61, 331–349 (1989).

    Article  CAS  PubMed  Google Scholar 

  18. Watanabe, M. Prefrontal unit activity during delayed conditional Go/No-Go discrimination in the monkey. II. Relation to Go and No-Go responses. Brain Res. 382, 15–27 (1986).

    Article  CAS  PubMed  Google Scholar 

  19. Watanabe, M. Prefrontal unit activity during delayed conditional Go/No-Go discrimination in the monkey. I. Relation to the stimulus. Brain Res. 382, 1–14 (1986).

    Article  CAS  PubMed  Google Scholar 

  20. Freedman, D.J., Riesenhuber, M., Poggio, T. & Miller, E.K. Categorical representation of visual stimuli in the primate prefrontal cortex. Science 291, 312–316 (2001).

    Article  CAS  PubMed  Google Scholar 

  21. Jiang, Y., Haxby, J.V., Martin, A., Ungerleider, L.G. & Parasuraman, R. Complementary neural mechanisms for tracking items in human working memory. Science 287, 643–646 (2000).

    Article  CAS  PubMed  Google Scholar 

  22. Shulman, G.L., Ollinger, J.M., Linenweber, M., Petersen, S.E. & Corbetta, M. Multiple neural correlates of detection in the human brain. Proc. Natl. Acad. Sci. USA 98, 313–318 (2001).

    Article  CAS  PubMed  Google Scholar 

  23. Bichot, N.P., Schall, J.D. & Thompson, K.G. Visual feature selectivity in frontal eye fields induced by experience in mature macaques. Nature 381, 697–699 (1996).

    Article  CAS  PubMed  Google Scholar 

  24. 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  PubMed  Google Scholar 

  25. Moran, J. & Desimone, R. Selective attention gates visual processing in the extrastriate cortex. Science 229, 782–784 (1985).

    Article  CAS  PubMed  Google Scholar 

  26. Reynolds, J.H., Chelazzi, L. & Desimone, R. Competitive mechanisms subserve attention in macaque areas V2 and V4. J. Neurosci. 19, 1736–1753 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Roelfsema, P.R., Lamme, V.A.F. & Spekreijse, H. Object-based attention in the primary visual cortex of the macaque monkey. Nature 395, 376–381 (1998).

    Article  CAS  PubMed  Google Scholar 

  28. Treue, S. & Maunsell, J.H. Attentional modulation of visual motion processing in cortical areas MT and MST. Nature 382, 539–541 (1996).

    Article  CAS  PubMed  Google Scholar 

  29. Bushnell, M.C., Goldberg, M.E. & Robinson, D.L. Behavioral enhancement of visual responses in monkey cerebral cortex. I. Modulation in posterior parietal cortex related to selective visual attention. J. Neurophysiol. 46, 755–772 (1981).

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  31. Chelazzi, L., Duncan, J., Miller, E.K. & Desimone, R. Responses of neurons in inferior temporal cortex during memory-guided visual search. J. Neurophysiol. 80, 2918–2940 (1998).

    Article  CAS  PubMed  Google Scholar 

  32. Sato, T. Effects of attention and stimulus interaction on visual responses of inferior temporal neurons in macaque. J. Neurophysiol. 60, 344–364 (1988).

    Article  CAS  PubMed  Google Scholar 

  33. Seidemann, E. & Newsome, W.T. Effect of spatial attention on the responses of area MT neurons. J. Neurophysiol. 81, 1783–1794 (1999).

    Article  CAS  PubMed  Google Scholar 

  34. Baynes, K., Holtzman, J.D. & Volpe, B.T. Components of visual attention. Alterations in response pattern to visual stimuli following parietal lobe infarction. Brain 109, 99–114 (1986).

    Article  PubMed  Google Scholar 

  35. Duncan, J. et al. Systematic analysis of deficits in visual attention. J. Exp. Psychol. Gen. 128, 450–478 (1999).

    Article  CAS  PubMed  Google Scholar 

  36. Dell'Acqua, R., Turatto, M. & Jolicoeur, P. Cross-modal attentional deficits in processing tactile stimulation. Percept. Psychophys. 63, 777–789 (2001).

    Article  CAS  PubMed  Google Scholar 

  37. 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  PubMed  Google Scholar 

Download references

Acknowledgements

The authors thank E.K. Miller and T. Norden-Krichmar for assistance in setting up Cortex, W. Asaad for supplying the SpikeToolbox, and S. Mygdal and M. Brown for surgical assistance.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to John Duncan.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Everling, S., Tinsley, C., Gaffan, D. et al. Filtering of neural signals by focused attention in the monkey prefrontal cortex. Nat Neurosci 5, 671–676 (2002). https://doi.org/10.1038/nn874

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nn874

This article is cited by

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing