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:

Influence of the thalamus on spatial visual processing in frontal cortex

Nature volume 444, pages 374–377 (2006)Cite this article

Abstract

Each of our movements activates our own sensory receptors, and therefore keeping track of self-movement is a necessary part of analysing sensory input. One way in which the brain keeps track of self-movement is by monitoring an internal copy, or corollary discharge, of motor commands1,2,3,4,5,6,7,8,9,10,11,12,13. This concept could explain why we perceive a stable visual world despite our frequent quick, or saccadic, eye movements: corollary discharge about each saccade would permit the visual system to ignore saccade-induced visual changes6,7,8,9. The critical missing link has been the connection between corollary discharge and visual processing. Here we show that such a link is formed by a corollary discharge from the thalamus that targets the frontal cortex. In the thalamus, neurons in the mediodorsal nucleus relay a corollary discharge of saccades from the midbrain superior colliculus to the cortical frontal eye field10,11,12. In the frontal eye field, neurons use corollary discharge to shift their visual receptive fields spatially before saccades14,15. We tested the hypothesis that these two components—a pathway for corollary discharge and neurons with shifting receptive fields—form a circuit in which the corollary discharge drives the shift. First we showed that the known spatial and temporal properties of the corollary discharge predict the dynamic changes in spatial visual processing of cortical neurons when saccades are made. Then we moved from this correlation to causation by isolating single cortical neurons and showing that their spatial visual processing is impaired when corollary discharge from the thalamus is interrupted. Thus the visual processing of frontal neurons is spatiotemporally matched with, and functionally dependent on, corollary discharge input from the thalamus. These experiments establish the first link between corollary discharge and visual processing, delineate a brain circuit that is well suited for mediating visual stability, and provide a framework for studying corollary discharge in other sensory systems.

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: Shifting receptive fields of visual neurons.
Figure 2: The spatial properties of shifting RFs are predicted by corollary discharge from the SC–MD–FEF pathway.
Figure 3: The temporal properties of shifting RFs are predicted by corollary discharge from the SC–MD–FEF pathway.
Figure 4: Shifting RFs require corollary discharge from the pathway.

Similar content being viewed by others

References

  1. Teuber, H.-L. in The Frontal Granular Cortex and Behavior (eds Warren, J. P. & Akerts, K.) 410–444 (McGraw-Hill, New York, 1964)

    Google Scholar 

  2. Delcomyn, F. Corollary discharge to cockroach giant interneurons. Nature 269, 160–162 (1977)

    Article  ADS  CAS  Google Scholar 

  3. Poulet, J. F. & Hedwig, B. A corollary discharge maintains auditory sensitivity during sound production. Nature 418, 872–876 (2002)

    Article  ADS  CAS  Google Scholar 

  4. Bell, C. C. in Comparative Physiology: Sensory Systems (eds Bolis, L. & Keynes, R. D.) 637–646 (Cambridge Univ. Press, Cambridge, 1984)

    Google Scholar 

  5. Thier, P., Haarmeier, T., Chakraborty, S., Lindner, A. & Tikhonov, A. Cortical substrates of perceptual stability during eye movements. Neuroimage 14, S33–S39 (2001)

    Article  CAS  Google Scholar 

  6. Wurtz, R. H. & Sommer, M. A. Identifying corollary discharges for movement in the primate brain. Prog. Brain Res. 144, 47–60 (2004)

    Article  Google Scholar 

  7. Von Helmholtz, H. Helmholtz’s Treatise on Physiological Optics (Thoemmes, Bristol, 2000)

    Google Scholar 

  8. Sperry, R. W. Neural basis of the spontaneous optokinetic response produced by visual inversion. J. Comp. Physiol. Psychol. 43, 482–489 (1950)

    Article  CAS  Google Scholar 

  9. Von Holst, E. & Mittelstaedt, H. Das Reafferenzprinzip. Wechselwirkungen zwischen Zentralnervensystem und Peripherie. Naturwissenschaften 37, 464–476 (1950)

    Article  ADS  Google Scholar 

  10. Sommer, M. A. & Wurtz, R. H. What the brain stem tells the frontal cortex. I. Oculomotor signals sent from superior colliculus to frontal eye field via mediodorsal thalamus. J. Neurophysiol. 91, 1381–1402 (2004)

    Article  Google Scholar 

  11. Sommer, M. A. & Wurtz, R. H. What the brain stem tells the frontal cortex. II. Role of the SC–MD–FEF pathway in corollary discharge. J. Neurophysiol. 91, 1403–1423 (2004)

    Article  Google Scholar 

  12. Sommer, M. A. & Wurtz, R. H. A pathway in primate brain for internal monitoring of movements. Science 296, 1480–1482 (2002)

    Article  ADS  CAS  Google Scholar 

  13. Guthrie, B. L., Porter, J. D. & Sparks, D. L. Corollary discharge provides accurate eye position information to the oculomotor system. Science 221, 1193–1195 (1983)

    Article  ADS  CAS  Google Scholar 

  14. Umeno, M. M. & Goldberg, M. E. Spatial processing in the monkey frontal eye field. I. Predictive visual responses. J. Neurophysiol. 78, 1373–1383 (1997)

    Article  CAS  Google Scholar 

  15. Umeno, M. M. & Goldberg, M. E. Spatial processing in the monkey frontal eye field. II. Memory responses. J. Neurophysiol. 86, 2344–2352 (2001)

    Article  CAS  Google Scholar 

  16. Duhamel, J. R., Colby, C. L. & Goldberg, M. E. The updating of the representation of visual space in parietal cortex by intended eye movements. Science 255, 90–92 (1992)

    Article  ADS  CAS  Google Scholar 

  17. Kusunoki, M. & Goldberg, M. E. The time course of perisaccadic receptive field shifts in the lateral intraparietal area of the monkey. J. Neurophysiol. 89, 1519–1527 (2003)

    Article  Google Scholar 

  18. Nakamura, K. & Colby, C. L. Updating of the visual representation in monkey striate and extrastriate cortex during saccades. Proc. Natl Acad. Sci. USA 99, 4026–4031 (2002)

    Article  ADS  CAS  Google Scholar 

  19. Sparks, D. L. & Hartwich-Young, R. in The Neurobiology of Saccadic Eye Movements; Reviews of Oculomotor Research Vol. III (eds Wurtz, R. H. & Goldberg, M. E.) 213–255 (Elsevier, Amsterdam, 1989)

    Google Scholar 

  20. Hanes, D. P. & Schall, J. D. Countermanding saccades in macaque. Vis. Neurosci. 12, 929–937 (1995)

    Article  CAS  Google Scholar 

  21. Lomber, S. G. The advantages and limitations of permanent or reversible deactivation techniques in the assessment of neural function. J. Neurosci. Methods 86, 109–117 (1999)

    Article  CAS  Google Scholar 

  22. Sommer, M. A. & Wurtz, R. H. Composition and topographic organization of signals sent from the frontal eye field to the superior colliculus. J. Neurophysiol. 83, 1979–2001 (2000)

    Article  CAS  Google Scholar 

  23. Lynch, J. C., Hoover, J. E. & Strick, P. L. Input to the primate frontal eye field from the substantia nigra, superior colliculus, and dentate nucleus demonstrated by transneuronal transport. Exp. Brain Res. 100, 181–186 (1994)

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This research was supported by the Intramural Research Program of the NIH and the NEI. Author Contributions Both authors designed the experiments, M.A.S. performed and analysed them, and both authors wrote the paper.

Author information

Authors and Affiliations

  1. Department of Neuroscience, the Center for the Neural Basis of Cognition, and the Center for Neuroscience at the University of Pittsburgh, University of Pittsburgh, Pennsylvania, 15260, Pittsburgh, USA

    Marc A. Sommer

  2. Laboratory of Sensorimotor Research, National Eye Institute, NIH, Bethesda, Maryland, 20892, USA

    Marc A. Sommer & Robert H. Wurtz

Authors
  1. Marc A. Sommer
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Robert H. Wurtz
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Marc A. Sommer.

Ethics declarations

Competing interests

Reprints and permissions information is available at www.nature.com/reprints. The authors declare no competing financial interests.

Supplementary information

Supplementary Notes

This file contains Supplementary Methods, Supplementary Notes, Supplementary References, Supplementary Discussion, and Supplementary Figures 1–8. (PDF 2365 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sommer, M., Wurtz, R. Influence of the thalamus on spatial visual processing in frontal cortex. Nature 444, 374–377 (2006). https://doi.org/10.1038/nature05279

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature05279

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