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Attention deficits without cortical neuronal deficits


The ability to process relevant stimuli selectively is a fundamental function of the primate visual system. The best-understood correlate of this function is the enhanced response of neurons in the visual cortex to attended stimuli1,2. However, recent results show that the superior colliculus (SC), a midbrain structure, also has a crucial role in visual attention3,4,5. It has been assumed that the SC acts through the same well-known mechanisms in the visual cortex3,5. Here we tested this hypothesis by transiently inactivating the SC during a motion-change-detection task and measuring responses in two visual cortical areas. We found that despite large deficits in visual attention, the enhanced responses of neurons in the visual cortex to attended stimuli were unchanged. These results show that the SC contributes to visual attention through mechanisms that are independent of the classic effects in the visual cortex, demonstrating that other processes must have key roles in visual attention.

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Figure 1: Task design and behavioural performance.
Figure 2: Sample neuronal activity before and during SC inactivation.
Figure 3: Population results before and during SC inactivation.


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

    CAS  Article  Google Scholar 

  2. Reynolds, J. H. & Chelazzi, L. Attentional modulation of visual processing. Annu. Rev. Neurosci. 27, 611–647 (2004)

    CAS  Article  Google Scholar 

  3. Müller, J. R., Philiastides, M. G. & Newsome, W. T. Microstimulation of the superior colliculus focuses attention without moving the eyes. Proc. Natl Acad. Sci. USA 102, 524–529 (2005)

    Article  ADS  Google Scholar 

  4. Lovejoy, L. P. & Krauzlis, R. J. Inactivation of primate superior colliculus impairs covert selection of signals for perceptual judgments. Nature Neurosci. 13, 261–266 (2010)

    CAS  Article  Google Scholar 

  5. Cavanaugh, J. Subcortical modulation of attention counters change blindness. J. Neurosci. 24, 11236–11243 (2004)

    CAS  Article  Google Scholar 

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

    CAS  Article  ADS  Google Scholar 

  7. Treue, S. Neural correlates of attention in primate visual cortex. Trends Neurosci. 24, 295–300 (2001)

    CAS  Article  Google Scholar 

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

    CAS  Article  ADS  Google Scholar 

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

    CAS  Article  Google Scholar 

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

    CAS  Article  ADS  Google Scholar 

  11. Ignashchenkova, A., Dicke, P. W., Haarmeier, T. & Thier, P. Neuron-specific contribution of the superior colliculus to overt and covert shifts of attention. Nature Neurosci. 7, 56–64 (2003)

    Article  Google Scholar 

  12. O’Connor, D. H., Fukui, M. M., Pinsk, M. A. & Kastner, S. Attention modulates responses in the human lateral geniculate nucleus. Nature Neurosci. 5, 1203–1209 (2002)

    Article  Google Scholar 

  13. Bender, D. B. & Youakim, M. Effect of attentive fixation in macaque thalamus and cortex. J. Neurophysiol. 85, 219–234 (2001)

    CAS  Article  Google Scholar 

  14. Robinson, D. L. & Petersen, S. E. The pulvinar and visual salience. Trends Neurosci. 15, 127–132 (1992)

    CAS  Article  Google Scholar 

  15. Rudolph, K. Transient and permanent deficits in motion perception after lesions of cortical areas MT and MST in the macaque monkey. Cereb. Cortex 9, 90–100 (1999)

    CAS  Article  Google Scholar 

  16. Treue, S. & Maunsell, J. H. R. Attentional modulation of visual motion processing in cortical areas MT and MST. Nature 382, 539–541 (1996)

    CAS  Article  ADS  Google Scholar 

  17. Hafed, Z. M., Goffart, L. & Krauzlis, R. J. Superior colliculus inactivation causes stable offsets in eye position during tracking. J. Neurosci. 28, 8124–8137 (2008)

    CAS  Article  Google Scholar 

  18. Hanley, J. A. & McNeil, B. J. The meaning and use of the area under a receiver operating characteristic (ROC) curve. Radiology 143, 29–36 (1982)

    CAS  Article  Google Scholar 

  19. Mitchell, J. F., Sundberg, K. A. & Reynolds, J. H. Differential attention-dependent response modulation across cell classes in macaque visual area V4. Neuron 55, 131–141 (2007)

    CAS  Article  Google Scholar 

  20. Cohen, M. R. & Maunsell, J. H. R. Attention improves performance primarily by reducing interneuronal correlations. Nature Neurosci. 12, 1594–1600 (2009)

    CAS  Article  Google Scholar 

  21. Mitchell, J. F., Sundberg, K. A. & Reynolds, J. H. Spatial attention decorrelates intrinsic activity fluctuations in macaque area V4. Neuron 63, 879–888 (2009)

    CAS  Article  Google Scholar 

  22. Moore, T. The neurobiology of visual attention: finding sources. Curr. Opin. Neurobiol. 16, 159–165 (2006)

    CAS  Article  Google Scholar 

  23. Redgrave, P., Prescott, T. J. & Gurney, K. The basal ganglia: a vertebrate solution to the selection problem? Neuroscience 89, 1009–1023 (1999)

    CAS  Article  Google Scholar 

  24. Moore, T. & Armstrong, K. M. Selective gating of visual signals by microstimulation of frontal cortex. Nature 421, 370–373 (2003)

    CAS  Article  ADS  Google Scholar 

  25. Wardak, C., Ibos, G., Duhamel, J.-R. & Olivier, E. Contribution of the monkey frontal eye field to covert visual attention. J. Neurosci. 26, 4228–4235 (2006)

    CAS  Article  Google Scholar 

  26. Treue, S. & Martínez Trujillo, J. C. Feature-based attention influences motion processing gain in macaque visual cortex. Nature 399, 575–579 (1999)

    CAS  Article  ADS  Google Scholar 

  27. Carrasco, M., Ling, S. & Read, S. Attention alters appearance. Nature Neurosci. 7, 308–313 (2004)

    CAS  Article  Google Scholar 

  28. Rensink, R. A., O’Regan, J. K. & Clark, J. J. To see or not to see: the need for attention to perceive changes in scenes. Psychol. Sci. 8, 368–373 (1997)

    Article  Google Scholar 

  29. Ross, T. D. Accurate confidence intervals for binomial proportion and Poisson rate estimation. Comput. Biol. Med. 33, 509–531 (2003)

    Article  Google Scholar 

  30. Palmer, J. & Moore, C. M. Using a filtering task to measure the spatial extent of selective attention. Vision Res. 49, 1045–1064 (2009)

    Article  Google Scholar 

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

    CAS  Article  Google Scholar 

  32. Dickey, A. S., Suminski, A., Amit, Y. & Hatsopoulos, N. G. Single-unit stability using chronically implanted multielectrode arrays. J. Neurophysiol. 102, 1331–1339 (2009)

    Article  Google Scholar 

  33. Schoppmann, A. & Hoffmann, K. P. Continuous mapping of direction selectivity in the cat’s visual cortex. Neurosci. Lett. 2, 177–181 (1976)

    CAS  Article  Google Scholar 

  34. Berger, J. & Pericchi, L. in Model Selection Vol 38 (ed. Lahiri, P ) 135–207 (Institute of Mathematical Statistics Lecture Notes – Monograph Series, 2001)

    Book  Google Scholar 

  35. Wagenmakers, E. J. A practical solution to the pervasive problems of p values. Psychon. Bull. Rev. 14, 779–804 (2007)

    Article  Google Scholar 

  36. Wetzelsls, R., Raaijmakers, J. G. W., Jakab, E. & Wagenmakers, E. J. How to quantify support for and against the null hypothesis: a flexible WinBUGS implementation of a default Bayesian t test. Psychon. Bull. Rev. 16, 752–760 (2009)

    Article  Google Scholar 

  37. Bair, W., Zohary, E. & Newsome, W. T. Correlated firing in macaque visual area MT: time scales and relationship to behavior. J. Neurosci. 21, 1676–1697 (2001)

    CAS  Article  Google Scholar 

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We thank E. Boehle, N. Dill and A. Karnik for technical assistance, and R. Wurtz for discussions and reading of the manuscript. This work was supported by the F.M. Kirby Foundation and the National Eye Institute Intramural Research Program at the National Institutes of Health.

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Authors and Affiliations



A.Z. and R.J.K. designed and conducted the experiments and wrote the manuscript. A.Z. analysed the data.

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Correspondence to Richard J. Krauzlis.

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The authors declare no competing financial interests.

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Zénon, A., Krauzlis, R. Attention deficits without cortical neuronal deficits. Nature 489, 434–437 (2012).

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