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.

  • Letter
  • Published:

Gaze direction controls response gain in primary visual-cortex neurons

Nature volume 398, pages 239–242 (1999)Cite this article

Abstract

To localize objects in space, the brain needs to combine information about the position of the stimulus on the retinae with information about the location of the eyes in their orbits. Interaction between these two types of information occurs in several cortical areas1,2,3,4,5,6,7,8,9,10,11,12, but the role of the primary visual cortex (area V1) in this process has remained unclear. Here we show that, for half the cells recorded in area V1 of behaving monkeys, the classically described visual responses are strongly modulated by gaze direction. Specifically, we find that selectivity for horizontal retinal disparity—the difference in the position of a stimulus on each retina which relates to relative object distance—and for stimulus orientation may be present at a given gaze direction, but be absent or poorly expressed at another direction. Shifts in preferred disparity also occurred in several neurons. These neural changes were most often present at the beginning of the visual response, suggesting a feedforward gain control by eye position signals. Cortical neural processes for encoding information about the three-dimensional position of a stimulus in space therefore start as early as area V1.

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: Experimental set-up.
Figure 2: Retinal disparity tuning curves obtained in three individual neurons at three directions of gaze (−10°, green; 0°, red; +10°, blue).
Figure 3: Effects of changing gaze direction on the responses of three individual neurons to oriented stimuli.
Figure 4: Distributions of the modulation index.
Figure 5: Time course of visual responses.

Similar content being viewed by others

References

  1. Andersen, R. A. & Mountcastle, V. M. The influence of the angle of gaze upon the excitability of the light-sensitive neurons of the posterior parietal cortex. J. Neurosci. 3, 532–548 (1983).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Andersen, R. A., Essick, G. K. & Siegel, R. M. Encoding of spatial location by posterior parietal neurons. Science 230, 456–458 (1985).

    Article  ADS  CAS  PubMed  Google Scholar 

  3. Andersen, R. A., Bracewell, R. M., Barash, S., Gnadt, J. W. & Fogassi, L. Eye position effects on visual, memory and saccade-related activity in areas LIP and 7A of macaque. J. Neurosci. 10, 1176–1196 (1990).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Squatrito, S. & Maioli, M. G. Gaze field properties of eye position neurones in areas MST and 7a of the macaque monkey. Vis. Neurosci. 13, 385–398 (1996).

    Article  CAS  PubMed  Google Scholar 

  5. Galletti, C. & Battaglini, P. P. Gaze-dependent visual neurons in area V3A of monkey prestriate cortex. J. Neurosci. 9, 1112–1125 (1989).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Galletti, C., Battaglini, P. P. & Fattori, P. Eye position influence on the parieto-occipital area PO (V6) of the macaque monkey. Eur. J. Neurosci. 7, 2486–2501 (1995).

    Article  CAS  PubMed  Google Scholar 

  7. Weyand, T. G. & Malpeli, J. G. Responses of neurons in primary visual cortex are modulated by eye position. J. Neurophysiol. 69, 2258–2260 (1993).

    Article  CAS  PubMed  Google Scholar 

  8. Guo, K. & Li, C. Y. Eye position-dependent activation of neurones in striate cortex of macaque. NeuroReport 8, 1405–1409 (1997).

    Article  CAS  PubMed  Google Scholar 

  9. Newsome, W. T., Wurtz, R. H. & Komatsu, H. Relation of cortical areas MT and MST to pursuit eye movements. II. Differentation of retinal from extraretinal inputs. J. Neurophysiol. 60, 604–644 (1988).

    Article  CAS  PubMed  Google Scholar 

  10. Duhamel, J. R., Bremmer, F., BenHamed, S. & Graf, W. Spatial invariance of visual receptive fields in parietal cortex neurons. Nature 389, 845–848 (1998).

    Article  ADS  Google Scholar 

  11. Boussaoud, D., Barth, T. M. & Wise, S. P. Effect of gaze on apparent visual responses of monkey frontal cortex neurons. Exp. Brain. Res. 93, 423–434 (1993).

    Article  CAS  PubMed  Google Scholar 

  12. Graziano, M. S. A., Hu, X. T. & Gross, C. G. Visuospatial properties of ventral premotor cortex. J. Neurophysiol. 77, 2268–2292 (1997).

    Article  CAS  PubMed  Google Scholar 

  13. Hubel, T. & Wiesel, T. N. Receptor fields and functional architecture of monkey striate cortex. J. Physiol. (Lond.) 195, 215–243 (1968).

    Article  CAS  Google Scholar 

  14. Barlow, H. B., Blakemore, C. D. & Pettigrew, J. D. The neural mechanism of binocular depth discrimination. J. Physiol. (Lond.) 193, 327–342 (1967).

    Article  CAS  Google Scholar 

  15. Poggio, G. F. & Fischer, B. Binocular interaction and depth sensitivity in striate and prestriate cortex of behaving rhesus monkeys. J. Neurophysiol. 40, 1392–1407 (1977).

    Article  CAS  PubMed  Google Scholar 

  16. Trotter, Y., Celebrini, S., Stricanne, B., Thorpe, S. & Imbert, M. Modulation of neural stereoscopic processing in primate area V1 by the viewing distance. Science 257, 1279–1281 (1992).

    Article  ADS  CAS  PubMed  Google Scholar 

  17. Trotter, Y., Celebrini, S., Stricanne, B., Thorpe, S. & Imbert, M. Neural processing of stereopsis as a function of viewing distance in primate visual cortical area V1. J. Neurophysiol. 76, 2872–2885 (1996).

    Article  CAS  PubMed  Google Scholar 

  18. Ogle, K. N. in Spatial Localization Through Binocular Vision (ed. Davson, H.) 271–324 (Academic, New York, (1962).

    Google Scholar 

  19. Ogle, K. N. in The Problem of the Horopter (ed. Davson, H.) 325–348 (Academic, New York, (1962).

    Google Scholar 

  20. Morrison, L. C. Stereoscopic localization with the eyes asymmetrically converged. Am. J. Optom. Physiol. Optics 54, 556–566 (1977).

    Article  CAS  Google Scholar 

  21. Zipser, D. & Andersen, R. A. Aback-propagation programmed network that simulates response properties of a subset of posterior parietal neurons. Nature 331, 679–684 (1988).

    Article  ADS  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Donaldson, I. M. L. & Dixon, R. A. Excitation of units in the lateral geniculate and contiguous nuclei of the cat by stretch of extrinsic ocular muscles. Exp. Brain Res. 38, 245–255 (1980).

    Article  CAS  PubMed  Google Scholar 

  24. Molotchnikoff, S. & Casanova, C. Reactions of the geniculate cells to extraocular proprioceptive activation in rabbits. J. Neurosci. Res. 14, 105–115 (1985).

    Article  CAS  PubMed  Google Scholar 

  25. Lal, R. & Friedlander, M. J. Gating of retinal transmission by afferent eye position and movement signals. Science 243, 93–96 (1989).

    Article  ADS  CAS  PubMed  Google Scholar 

  26. Motter, B. C. 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  PubMed  Google Scholar 

  27. Gilbert, C. D. Adult cortical dynamics. Physiol. Rev. 78, 467–485 (1998).

    Article  ADS  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank J. Bullier, Y. Frégnac and S. Thorpe for criticism of the manuscript; K.Britten for advice on various logistics; and M. Imbert for continuous support. This work was supported by the Centre National de la Recherche Scientifique.

Author information

Authors and Affiliations

  1. Centre de Recherche Cerveau et Cognition, Faculté de Médecine de Rangueil, Université Paul Sabatier, 133, route de Narbonne, 31062, Toulouse Cedex, France

    Yves Trotter & Simona Celebrini

Authors
  1. Yves Trotter
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Simona Celebrini
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yves Trotter.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Trotter, Y., Celebrini, S. Gaze direction controls response gain in primary visual-cortex neurons. Nature 398, 239–242 (1999). https://doi.org/10.1038/18444

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/18444

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

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