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:

Early involvement of prefrontal cortex in visual bottom-up attention

Nature Neuroscience volume 15, pages 1160–1166 (2012)Cite this article

Subjects

Abstract

Visual attention is guided to stimuli either on the basis of their intrinsic saliency against their background (bottom-up factors) or through willful search of known targets (top-down factors). Posterior parietal cortex (PPC) is thought to be important for the guidance of visual bottom-up attention, whereas dorsolateral prefrontal cortex is thought to represent top-down factors. Contrary to this established view, we found that, when monkeys were tested in a task requiring detection of a salient stimulus defined purely by bottom-up factors and whose identity was unknown before the presentation of a visual display, prefrontal neurons represented the salient stimulus no later than those in the PPC. This was true even though visual response latency was shorter in parietal than in prefrontal cortex. These results suggest an early involvement of the prefrontal cortex in the bottom-up guidance of visual attention.

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

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

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

Figure 1: Schematic diagram of the behavioral tasks and the monkey brain.
Figure 2: Behavioral response time as a function of stimulus set size.
Figure 3: Population firing rate.
Figure 4: ROC analysis and mutual information analysis.
Figure 5: Relationship between discriminability and time of target discrimination.
Figure 6: Population responses during the reaction-time task.
Figure 7: Population responses in the difficult-discrimination task.
Figure 8: ROC and mutual information analysis for responses in the difficult-discrimination task.

Similar content being viewed by others

References

  1. Bisley, J.W. & Goldberg, M.E. Attention, intention, and priority in the parietal lobe. Annu. Rev. Neurosci. 33, 1–21 (2010).

    Article  CAS  Google Scholar 

  2. Schall, J.D. The neural selection and control of saccades by the frontal eye field. Phil. Trans. R. Soc. Lond. B 357, 1073–1082 (2002).

    Article  Google Scholar 

  3. Noudoost, B., Chang, M.H., Steinmetz, N.A. & Moore, T. Top-down control of visual attention. Curr. Opin. Neurobiol. 20, 183–190 (2010).

    Article  CAS  Google Scholar 

  4. Connor, C.E., Egeth, H.E. & Yantis, S. Visual attention: bottom-up versus top-down. Curr. Biol. 14, R850–R852 (2004).

    Article  CAS  Google Scholar 

  5. Corbetta, M. & Shulman, G.L. Control of goal-directed and stimulus-driven attention in the brain. Nat. Rev. Neurosci. 3, 201–215 (2002).

    Article  CAS  Google Scholar 

  6. Ungerleider, L.G. & Mishkin, M. Two cortical visual systems. in Analysis of Visual Behavior (eds. Ingle, D.J., Goodale, M.A. & Mansfield, R.J.W.) 549–586 (MIT Press, 1982).

  7. Felleman, D.J. & Van Essen, D.C. Distributed hierarchical processing in the primate cerebral cortex. Cereb. Cortex 1, 1–47 (1991).

    Article  CAS  Google Scholar 

  8. Serre, T., Oliva, A. & Poggio, T. A feedforward architecture accounts for rapid categorization. Proc. Natl. Acad. Sci. USA 104, 6424–6429 (2007).

    Article  CAS  Google Scholar 

  9. Buschman, T.J. & Miller, E.K. Top-down versus bottom-up control of attention in the prefrontal and posterior parietal cortices. Science 315, 1860–1862 (2007).

    Article  CAS  Google Scholar 

  10. Kustov, A.A. & Robinson, D.L. Shared neural control of attentional shifts and eye movements. Nature 384, 74–77 (1996).

    Article  CAS  Google Scholar 

  11. Moore, T. & Fallah, M. Control of eye movements and spatial attention. Proc. Natl. Acad. Sci. USA 98, 1273–1276 (2001).

    Article  CAS  Google Scholar 

  12. Constantinidis, C. & Steinmetz, M.A. Neuronal responses in area 7a to multiple stimulus displays. I. Neurons encode the location of the salient stimulus. Cereb. Cortex 11, 581–591 (2001).

    Article  CAS  Google Scholar 

  13. Schall, J.D. & Hanes, D.P. Neural basis of saccade target selection in frontal eye field during visual search. Nature 366, 467–469 (1993).

    Article  CAS  Google Scholar 

  14. Preuss, T.M. & Goldman-Rakic, P.S. Myelo- and cytoarchitecture of the granular frontal cortex and surrounding regions in the strepsirhine primate Galago and the anthropoid primate Macaca. J. Comp. Neurol. 310, 429–474 (1991).

    Article  CAS  Google Scholar 

  15. Badre, D. & D'Esposito, M. Is the rostro-caudal axis of the frontal lobe hierarchical? Nat. Rev. Neurosci. 10, 659–669 (2009).

    Article  CAS  Google Scholar 

  16. Sato, T.R., Watanabe, K., Thompson, K.G. & Schall, J.D. Effect of target-distractor similarity on FEF visual selection in the absence of the target. Exp Brain Res 151, 356–363 (2003).

    Article  Google Scholar 

  17. Treisman, A.M. & Gelade, G. A feature-integration theory of attention. Cognit. Psychol. 12, 97–136 (1980).

    Article  CAS  Google Scholar 

  18. Wolfe, J.M. Guided Search 2.0. A revised model of visual search. Psychon. Bull. Rev. 1, 202–238 (1994).

    Article  CAS  Google Scholar 

  19. Itti, L. & Koch, C. Computational modeling of visual attention. Nat. Rev. Neurosci. 2, 194–203 (2001).

    Article  CAS  Google Scholar 

  20. Knierim, J.J. & van Essen, D.C. Neuronal responses to static texture patterns in area V1 of the alert macaque monkey. J. Neurophysiol. 67, 961–980 (1992).

    Article  CAS  Google Scholar 

  21. Hegdé, J. & Felleman, D.J. How selective are V1 cells for pop-out stimuli? J. Neurosci. 23, 9968–9980 (2003).

    Article  Google Scholar 

  22. Burrows, B.E. & Moore, T. Influence and limitations of popout in the selection of salient visual stimuli by area V4 neurons. J. Neurosci. 29, 15169–15177 (2009).

    Article  CAS  Google Scholar 

  23. Koch, C. & Ullman, S. Shifts in selective visual attention: towards the underlying neural circuitry. Hum. Neurobiol. 4, 219–227 (1985).

    CAS  PubMed  Google Scholar 

  24. Niebur, E. & Koch, C. Control of selective visual attention: modeling the “where” pathway. in Neural Information Processing Systems (eds. Touretzky, D.S., Mozer, M.C. & Hasselmo, M.E.) 802–808 (MIT Press, 1996).

  25. Katsuki, F. & Constantinidis, C. Unique and shared roles of the posterior parietal and dorsolateral prefrontal cortex in cognitive functions. Front. Integr. Neurosci. 6, 17 (2012).

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  27. McPeek, R.M. & Keller, E.L. Saccade target selection in the superior colliculus during a visual search task. J. Neurophysiol. 88, 2019–2034 (2002).

    Article  Google Scholar 

  28. Thomas, N.W. & Pare, M. Temporal processing of saccade targets in parietal cortex area LIP during visual search. J. Neurophysiol. 97, 942–947 (2007).

    Article  Google Scholar 

  29. 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 

  30. Wardak, C., Vanduffel, W. & Orban, G.A. Searching for a salient target involves frontal regions. Cereb. Cortex 20, 2464–2477 (2010).

    Article  Google Scholar 

  31. Cavada, C. & Goldman-Rakic, P.S. Posterior parietal cortex in rhesus monkey. II. Evidence for segregated corticocortical networks linking sensory and limbic areas with the frontal lobe. J. Comp. Neurol. 287, 422–445 (1989).

    Article  CAS  Google Scholar 

  32. Constantinidis, C. Posterior parietal mechanisms of visual attention. Rev. Neurosci. 17, 415–427 (2006).

    Article  Google Scholar 

  33. Arcizet, F., Mirpour, K. & Bisley, J.W. A pure salience response in posterior parietal cortex. Cereb. Cortex 21, 2498–2506 (2011).

    Article  Google Scholar 

  34. Premereur, E., Vanduffel, W. & Janssen, P. Functional heterogeneity of macaque lateral intraparietal neurons. J. Neurosci. 31, 12307–12317 (2011).

    Article  CAS  Google Scholar 

  35. 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  Google Scholar 

  36. Constantinidis, C. & Steinmetz, M.A. Posterior parietal cortex automatically encodes the location of salient stimuli. J. Neurosci. 25, 233–238 (2005).

    Article  CAS  Google Scholar 

  37. Meyer, T. & Constantinidis, C. A software solution for the control of visual behavioral experimentation. J. Neurosci. Methods 142, 27–34 (2005).

    Article  Google Scholar 

  38. Brainard, D.H. The Psychophysics Toolbox. Spat. Vis. 10, 433–436 (1997).

    Article  CAS  Google Scholar 

  39. Cavada, C. & Goldman-Rakic, P.S. Posterior parietal cortex in rhesus monkey. I. Parcellation of areas based on distinctive limbic and sensory corticocortical connections. J. Comp. Neurol. 287, 393–421 (1989).

    Article  CAS  Google Scholar 

  40. Harris, K.D., Henze, D.A., Csicsvari, J., Hirase, H. & Buzsaki, G. Accuracy of tetrode spike separation as determined by simultaneous intracellular and extracellular measurements. J. Neurophysiol. 84, 401–414 (2000).

    Article  CAS  Google Scholar 

  41. White, B.J. & Munoz, D.P. Separate visual signals for saccade initiation during target selection in the primate superior colliculus. J. Neurosci. 31, 1570–1578 (2011).

    Article  CAS  Google Scholar 

  42. Davison, A.C. & Hinkley, D.V. Bootstrap Methods and Their Application (Cambridge University Press, 1997).

  43. Rowland, B.A., Quessy, S., Stanford, T.R. & Stein, B.E. Multisensory integration shortens physiological response latencies. J. Neurosci. 27, 5879–5884 (2007).

    Article  CAS  Google Scholar 

  44. Tolhurst, D.J., Movshon, J.A. & Dean, A.F. The statistical reliability of signals in single neurons in cat and monkey visual cortex. Vision Res. 23, 775–785 (1983).

    Article  CAS  Google Scholar 

  45. Dayan & Abbott, L.F. Theoretical Neuroscience: Computational and Mathematical Modeling of Neural Systems (The MIT Press, 2001).

Download references

Acknowledgements

We wish to thank K. Palaninathan, K. Roberts and J. Rawley for helping with the experiments, and R. Ramachandran, T. Stanford and E. Salinas for comments. This work was supported by the National Eye Institute of the US National Institutes of Health under award number R01 EY016773 and by the Tab Williams Family Endowment Fund.

Author information

Authors and Affiliations

  1. Department of Neurobiology and Anatomy, Wake Forest University School of Medicine, Winston-Salem, North Carolina, USA

    Fumi Katsuki & Christos Constantinidis

Authors
  1. Fumi Katsuki
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Christos Constantinidis
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

F.K. and C.C. designed the experiments. F.K. performed the experiments. F.K. and C.C. analyzed the data and wrote the paper.

Corresponding author

Correspondence to Christos Constantinidis.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Text and Figures

Supplementary Figures 1–10 (PDF 6450 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Katsuki, F., Constantinidis, C. Early involvement of prefrontal cortex in visual bottom-up attention. Nat Neurosci 15, 1160–1166 (2012). https://doi.org/10.1038/nn.3164

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nn.3164

This article is cited by

Search

Advanced 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