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.

Attentional modulation in visual cortex depends on task timing

Abstract

Paying attention to a stimulus selectively increases the ability to process it. For example, when subjects attend to a specific region of a visual scene, their sensitivity to changes at that location increases. A large number of studies describe the behavioural consequences and neurophysiological correlates of attending to spatial locations1,2,3,4,5,6,7,8. There has, in contrast, been little study of the allocation of attention over time9,10. Because subjects can anticipate predictable events with great temporal precision11,12,13,14,15, it seems probable that they might dynamically shift their attention when performing a familiar perceptual task whose constraints changed over time. We trained monkeys to respond to a stimulus change where the probability of occurrence changed over time. Recording from area V4 of the visual cortex in these animals, we found that the modulation of neuronal responses changed according to the probability of the change occurring at that instant. Thus, we show that the attentional modulation of sensory neurons reflects a subject's anticipation of the timing of behaviourally relevant events.

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

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

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

Figure 1: Orientation change detection task.
Figure 2: Dynamic attentional modulation in a V4 neuron.
Figure 3: Attentional dynamics change according to task timing.
Figure 4: Population attentional modulation with different stimuli.

Similar content being viewed by others

References

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

    Article  ADS  CAS  Google Scholar 

  2. Motter, B. Focal attention produces spatially selective processing in visual cortical areas V1, V2, and V4 in the presence of competing stimuli. J. Neurophysiol. 70, 909–919 (1993)

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  4. Luck, S., Chelazzi, L., Hillyard, S. & 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 

  5. Connor, C., Preddie, D., Gallant, J. & Van Essen, D. Spatial attention effects in macaque area V4. J. Neurosci. 17, 3201–3214 (1997)

    Article  CAS  Google Scholar 

  6. McAdams, C. & Maunsell, J. Effects of attention on orientation-tuning functions of single neurons in macaque cortical area V4. J. Neurosci. 19, 431–441 (1999)

    Article  CAS  Google Scholar 

  7. Treue, S. & Maunsell, J. Effects of attention on the processing of motion in macaque middle temporal and medial superior temporal visual cortical areas. J. Neurosci. 19, 7591–7602 (1999)

    Article  CAS  Google Scholar 

  8. Colby, C. & Goldberg, M. Space and attention in parietal cortex. Annu. Rev. Neurosci. 22, 319–349 (1999)

    Article  CAS  Google Scholar 

  9. Coull, J. T., Frith, C. D., Buchel, C. & Nobre, A. C. Orienting attention in time: behavioural and neuroanatomical distinction between exogenous and endogenous shifts. Neuropsychologia 38, 808–819 (2000)

    Article  CAS  Google Scholar 

  10. Nobre, A. C. Orienting attention to instants in time. Neuropsychologia 39, 1317–1328 (2001)

    Article  CAS  Google Scholar 

  11. Treisman, M., Faulkner, A., Naish, P. & Brogan, D. The internal clock: evidence for a temporal oscillator underlying time perception with some estimates of its characteristic frequency. Perception 19, 705–743 (1990)

    Article  CAS  Google Scholar 

  12. Zakay, D. & Block, R. The role of attention in time estimation processes in Time, Internal Clocks and Movement (eds Pastor, M. A. & Artieda, J.) 143–164 (Elsevier Science, New York, 1996)

    Chapter  Google Scholar 

  13. Harrington, D., Haaland, K. & Knight, R. Cortical networks underlying mechanisms of time perception. J. Neurosci. 18, 1085–1095 (1998)

    Article  CAS  Google Scholar 

  14. Westheimer, G. Visual signals used in time-interval discrimination. Vis. Neurosci. 17, 551–556 (2000)

    Article  CAS  Google Scholar 

  15. Migliore, M., Messineo, L., Cardaci, M. & Ayala, G. Quantitative modeling of perception and production of time intervals. J. Neurophysiol. 86, 2754–2760 (2001)

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  17. Spitzer, H., Desimone, R. & Moran, J. Increased attention enhances both behavioural and neuronal performance. Science 240, 338–340 (1988)

    Article  ADS  CAS  Google Scholar 

  18. Colby, C., Duhamel, J. & Goldberg, M. Visual, presaccadic, and cognitive activation of single neurons in monkey lateral intraparietal area. J. Neurophysiol. 76, 2841–2852 (1996)

    Article  CAS  Google Scholar 

  19. Steinmetz, M., Connor, C., Constantinidis, C. & McLaughlin, J. Covert attention suppresses neuronal responses in area 7a of the posterior parietal cortex. J. Neurophysiol. 72, 1020–1023 (1994)

    Article  CAS  Google Scholar 

  20. Constantinidis, C. & Steinmetz, M. Neuronal responses in area 7a to multiple stimulus displays: ii. responses are suppressed at the cued location. Cereb. Cortex 11, 592–597 (2001)

    Article  CAS  Google Scholar 

  21. Robinson, D., Bowman, E. & Kertzman, C. Covert orienting of attention in macaques. II. Contributions of parietal cortex. J. Neurophysiol. 74, 698–712 (1995)

    Article  CAS  Google Scholar 

  22. Krose, B. & Julesz, B. The control and speed of shifts of attention. Vision Res. 29, 1607–1619 (1989)

    Article  CAS  Google Scholar 

  23. Saarinen, J. & Julesz, B. The speed of attentional shifts in the visual field. Proc. Natl Acad. Sci. USA 88, 1812–1814 (1991)

    Article  ADS  CAS  Google Scholar 

  24. Verstraten, F., Cavanagh, P. & Labianca, A. Limits of attentive tracking reveal temporal properties of attention. Vision Res. 40, 3651–3664 (2000)

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by grants from the National Eye Institute and the Human Frontier Science Program. J.H.R.M. is an Investigator with the Howard Hughes Medical Institute. We thank D. Murray and T. Williford for assistance with the animals, and W. Bosking, E. Cook, R. A. Eatock, M. Shadlen, D. Sparks, T. Yang and T. Williford for comments on the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Geoffrey M. Ghose.

Ethics declarations

Competing interests

The authors declare that they have no competing financial interests.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ghose, G., Maunsell, J. Attentional modulation in visual cortex depends on task timing. Nature 419, 616–620 (2002). https://doi.org/10.1038/nature01057

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature01057

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

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