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:

Two distinct modes of sensory processing observed in monkey primary visual cortex (V1)

Nature Neuroscience volume 4, pages 304–310 (2001)Cite this article

Abstract

Even salient sensory stimuli are sometimes not detected. What goes wrong in the brain in that case? Here we show that a late (> 100-ms) component of the neural activity in the primary visual cortex of the monkey is selectively suppressed when stimuli are not seen. As there is evidence that this activity depends on feedback from extrastriate areas, these findings suggest a specific role for recurrent processing when stimuli are reaching a perceptual level. Further results show that this perceptual level is situated between purely sensory and decision or motor stages of processing.

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: Figure–ground display and sequence of visual stimulation.
Figure 2: Eye movements.
Figure 3: Receptive fields, stimuli and neural responses.
Figure 4: `Seen' versus `not seen' neural responses.
Figure 5: Different line lengths, perceptual saliency and contextual modulation.
Figure 6: `Seen' versus `not seen' neural responses for different levels of stimulus saliency.
Figure 7: Model and supporting evidence of stimulus and decision processing in the visual system, showing two distinct modes of sensory processing.

Similar content being viewed by others

References

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

    Google Scholar 

  2. 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 

  3. Shadlen, M. N. & Newsome W. T. Motion perception: seeing and deciding. Proc. Natl. Acad. Sci. USA 93, 628–633 (1996).

    Article  CAS  Google Scholar 

  4. Leon, M. I. & Shadlen, M. N. Exploring the neurophysiology of decisions. Neuron 21, 669–672 (1998).

    Article  CAS  Google Scholar 

  5. Schall, J. D. & Bichot, N. P. Neural correlates of visual and motor decision processes. Curr. Opin. Neurobiol. 8, 211–217 (1998).

    Article  CAS  Google Scholar 

  6. Platt, M. L. & Glimcher, P. W. Neural correlates of decision variables in parietal cortex. Nature 400, 233–238 (1999).

    Article  CAS  Google Scholar 

  7. Kim, J.-N. & Shadlen, M. N. Neural correlates of a decision in the dorsolateral prefrontal cortex of the macaque. Nat. Neurosci. 2, 176–185 (1999).

    Article  Google Scholar 

  8. Thompson, K. G. & Schall, J. D. The detection of visual signals by macaque frontal eye field during masking. Nat. Neurosci. 2, 283–288 (1999).

    Article  CAS  Google Scholar 

  9. Lamme, V. A. F. The neurophysiology of figure–ground segregation in primary visual cortex. J. Neurosci. 15, 1605–1615. (1995).

    Article  CAS  Google Scholar 

  10. Zipser, K., Lamme, V. A. F. & Schiller, P. H. Contextual modulation primary visual cortex. J. Neurosci. 16, 7376–7389 (1996).

    Article  CAS  Google Scholar 

  11. Moore, T., Rodman, H. R., Repp, A. B. & Gross C. G. Localization of visual stimuli after striate cortex damage in monkeys: parallels with human blindsight. Proc. Natl. Acad. Sci. USA 92, 8215–8218 (1995).

    Article  CAS  Google Scholar 

  12. Lamme, V. A. F., Zipser, K. & Spekreijse, H. Figure-ground activity in primary visual cortex is suppressed by anaesthesia. Proc. Natl. Acad. Sci. USA. 95, 3263–3268 (1998).

    Article  CAS  Google Scholar 

  13. Lamme, V. A. F., Rodriguez, V. & Spekreijse H. Separate processing dynamics for texture elements, boundaries and surfaces in primary visual cortex. Cereb. Cortex 9, 406–413 (1999).

    Article  CAS  Google Scholar 

  14. Allman, J. M., Miezin, F., & McGuiness, E. Stimulus specific responses from beyond the classical receptive field: Neurophysiological mechanisms for local-global comparisons in visual neurons. Ann. Rev. Neurosci. 8, 407–430 (1985).

    Article  CAS  Google Scholar 

  15. Gilbert, C. D. Circuitry, architecture and functional dynamics of visual cortex. Cereb. Cortex 3, 373–386 (1993).

    Article  CAS  Google Scholar 

  16. Sillito, A. M., Grieve, K. L., Jones, H. E., Cudeiro, J., & Davis, J. Visual cortical mechanisms detecting focal orientation discontinuities. Nature 378, 492–496 (1996).

    Article  Google Scholar 

  17. 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 

  18. Kapadia, M. K., Ito, M., Gilbert, C. D., & Westheimer G. Improvement in visual sensitivity by changes in local context: parallel studies in human observers and in V1 of alert monkeys. Neuron 15, 843–856 (1995).

    Article  CAS  Google Scholar 

  19. Polat, U., Mizobe, K., Pettet, M. W., Kasamatsu, T. & Norcia, A. M. Collinear stimuli regulate visual responses depending on cell's contrast threshold. Nature 391, 580–584 (1998).

    Article  CAS  Google Scholar 

  20. Gilbert, C. D. & Wiesel, T. N. The influence of contextual stimuli on the orientation selectivity of cells in primary visual cortex of the cat. Vision Res. 30, 1689–1701 (1990).

    Article  CAS  Google Scholar 

  21. Rossi, A. F., Rittenhouse, C. D. & Paradiso, M. The representation of brightness in primary visual cortex. Science 273, 1104–1107 (1996).

    Article  CAS  Google Scholar 

  22. Salin, P. & Bullier, J. Corticocortical connections in the visual system: Structure and function. Physiol. Rev. 75, 107–154 (1995).

    Article  CAS  Google Scholar 

  23. Payne, B. R., Lomber, S. G., Villa, A. E., & Bullier, J. Reversible deactivation of cerebral network components. Trends Neurosci. 19, 535–542 (1996).

    Article  CAS  Google Scholar 

  24. Lamme, V. A. F., Supèr, H. & Spekreijse, H. Feedforward, horizontal, and feedback processing in the visual cortex. Curr. Opin. Neurobiol. 8, 529–535 (1998).

    Article  CAS  Google Scholar 

  25. Hupé, J. M., James, A. C., Payne, B. R., Lomber, S. G., Girard, P. & Bullier, J. Cortical feedback improves discrimination between figure and background by V1, V2 and V3 neurons. Nature 394, 784–787 (1998).

    Article  Google Scholar 

  26. Schiller, P. H., Malpeli, J. G. & Schein S. J. Composition of geniculostriate input to superior colliculus of the Rhesus monkey. J. Neurophysiol. 42, 1124–1133 (1979).

    Article  CAS  Google Scholar 

  27. Nothdurft, H. C. Orientation sensitivity and texture segmentation in patterns with different line orientation. Vision Res. 25, 551–560 (1985).

    Article  CAS  Google Scholar 

  28. Desimone, R., & Duncan, J. Neural correlates of selective visual attention. Ann. Rev. Neurosci. 18, 193–222 (1995).

    Article  CAS  Google Scholar 

  29. Vidyasagar, T. R. Gating of neuronal responses in macaque primary visual cortex by an attentional spotlight. Neuroreport 9, 1947–1952 (1998).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  31. Shadlen, M. N., Britten, K. H., Newsome, W. T. & Movshon, J. A. A computational analysis of the relationship between neuronal and behavioural responses to visual motion. J. Neurosci. 16, 1486–1510 (1996).

    Article  CAS  Google Scholar 

  32. Nothdurft, H. C., Gallant, J. L. & Van Essen, D. C. Response modulation by texture surround in primate area V1: correlates of `popout' under anesthesia. Vis. Neurosci. 16, 15–34 (1999).

    Article  CAS  Google Scholar 

  33. Block, N. How can we find the neural correlate of consciousness. Trends Neurosci. 19, 456–459 (1996).

    Article  CAS  Google Scholar 

  34. Rock, I., Linnett, C. M., Grant, P. & Mack, A. Perception without attention: results of a new method. Cognit. Psychol. 24, 501–534 (1992).

    Article  Google Scholar 

  35. Pollen, D. A. On the neural correlates of visual perception. Cereb. Cortex 9, 4–19 (1999).

    Article  CAS  Google Scholar 

  36. Bour, L. J., Van Gisbergen, J. A. M., Bruijns, J. & Ottes, F. P. The double magnetic induction method for measuring eye movement - results in monkey and man. IEEE Trans. BME 31, 419–427 (1984).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank P. Brassinga, H. Meester, J. de Feiter and K. Brandsma for technical support. We thank C. Koch, M. Regan, P. Roelfsema, J. Schall and M. Shadlen for their comments on earlier versions of this paper. H. Supèr is supported by a grant from Medical Sciences (MW), which is subsidized by the Netherlands Organization for Scientific Research (NWO).

Author information

Authors and Affiliations

  1. Department of Visual System Analysis, Graduate School of Neurosciences, AMC, University of Amsterdam, PO Box 12011, Amsterdam, 1100 AA, The Netherlands

    Hans Supèr, Henk Spekreijse & Victor A. F. Lamme

  2. The Netherlands Ophthalmic Research Institute, Meibergdreef 49, Amsterdam, 1105 BA, The Netherlands

    Hans Supèr & Victor A. F. Lamme

Authors
  1. Hans Supèr
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Henk Spekreijse
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Victor A. F. Lamme
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Victor A. F. Lamme.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Supèr, H., Spekreijse, H. & Lamme, V. Two distinct modes of sensory processing observed in monkey primary visual cortex (V1). Nat Neurosci 4, 304–310 (2001). https://doi.org/10.1038/85170

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/85170

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