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Blindsight depends on the lateral geniculate nucleus

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Abstract

Injury to the primary visual cortex (V1) leads to the loss of visual experience. Nonetheless, careful testing shows that certain visually guided behaviours can persist even in the absence of visual awareness1,2,3,4. The neural circuits supporting this phenomenon, which is often termed blindsight, remain uncertain4. Here we demonstrate that the thalamic lateral geniculate nucleus (LGN) has a causal role in V1-independent processing of visual information. By comparing functional magnetic resonance imaging (fMRI) and behavioural measures with and without temporary LGN inactivation, we assessed the contribution of the LGN to visual functions of macaque monkeys (Macaca mulatta) with chronic V1 lesions. Before LGN inactivation, high-contrast stimuli presented to the lesion-affected visual field (scotoma) produced significant V1-independent fMRI activation in the extrastriate cortical areas V2, V3, V4, V5/middle temporal (MT), fundus of the superior temporal sulcus (FST) and lateral intraparietal area (LIP) and the animals correctly located the stimuli in a detection task. However, following reversible inactivation of the LGN in the V1-lesioned hemisphere, fMRI responses and behavioural detection were abolished. These results demonstrate that direct LGN projections to the extrastriate cortex have a critical functional contribution to blindsight. They suggest a viable pathway to mediate fast detection during normal vision.

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Figure 1: Experimental set-up.
Figure 2: Visual processing in V1-lesioned monkeys.
Figure 3: Role of the LGN in driving V1-independent visual processing.
Figure 4: Quantitative summary of mean fMRI activation levels.

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  • 15 July 2009

    A small correction was made to the Fig. 2 legend.

References

  1. Weiskrantz, L., Warrington, E. K. & Sanders, M. D. Visual capacity in the hemianopic field following a restricted occipital ablation. Brain 97, 709–728 (1974)

    Article  CAS  Google Scholar 

  2. Cowey, A. & Stoerig, P. Blindsight in monkeys. Nature 373, 247–249 (1995)

    Article  ADS  CAS  Google Scholar 

  3. Keating, E. G. Residual spatial vision in the monkey after removal of striate and preoccipital cortex. Brain Res. 187, 271–290 (1980)

    Article  CAS  Google Scholar 

  4. Cowey, A. The blindsight saga. Exp. Brain Res. 200, 3–24 (2010)

    Article  ADS  Google Scholar 

  5. Brewer, A. A., Press, W. A., Logothetis, N. K. & Wandell, B. A. Visual areas in macaque cortex measured using functional magnetic resonance imaging. J. Neurosci. 22, 10416–10426 (2002)

    Article  CAS  Google Scholar 

  6. Schmid, M. C., Panagiotaropoulos, T., Augath, M. A., Logothetis, N. K. & Smirnakis, S. M. Visually driven activation in macaque areas V2 and V3 without input from the primary visual cortex. PLoS ONE 4 e5527 10.1371/journal.pone.0005527 (2009)

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  7. Baseler, H. A., Morland, A. B. & Wandell, B. A. Topographic organization of human visual areas in the absence of input from primary cortex. J. Neurosci. 19, 2619–2627 (1999)

    Article  CAS  Google Scholar 

  8. Cowey, A. & Stoerig, P. Visual detection in monkeys with blindsight. Neuropsychologia 35, 929–939 (1997)

    Article  CAS  Google Scholar 

  9. Collins, C. E., Lyon, D. C. & Kaas, J. H. Responses of neurons in the middle temporal visual area after long-standing lesions of the primary visual cortex in adult new world monkeys. J. Neurosci. 23, 2251–2264 (2003)

    Article  CAS  Google Scholar 

  10. Campion, J., Latto, R. & Smith, Y. M. Is blindsight an effect of scattered light, spared cortex, and near-threshold vision? Behav. Brain Sci. 6, 423–447 (1983)

    Article  Google Scholar 

  11. Goebel, R., Muckli, L., Zanella, F. E., Singer, W. & Stoerig, P. Sustained extrastriate cortical activation without visual awareness revealed by fMRI studies of hemianopic patients. Vision Res. 41, 1459–1474 (2001)

    Article  CAS  Google Scholar 

  12. Rodman, H. R., Gross, C. G. & Albright, T. D. Afferent basis of visual response properties in area MT of the macaque. I. Effects of striate cortex removal. J. Neurosci. 9, 2033–2050 (1989)

    Article  CAS  Google Scholar 

  13. Sincich, L. C., Park, K. F., Wohlgemuth, M. J. & Horton, J. C. Bypassing V1: a direct geniculate input to area MT. Nature Neurosci. 7, 1123–1128 (2004)

    Article  CAS  Google Scholar 

  14. Bullier, J. & Kennedy, H. Projection of the lateral geniculate nucleus onto cortical area V2 in the macaque monkey. Exp. Brain Res. 53, 168–172 (1983)

    Article  CAS  Google Scholar 

  15. Cope, D. W., Hughes, S. W. & Crunelli, V. GABAA receptor-mediated tonic inhibition in thalamic neurons. J. Neurosci. 25, 11553–11563 (2005)

    Article  CAS  Google Scholar 

  16. Curcio, C. A. & Allen, K. A. Topography of ganglion cells in human retina. J. Comp. Neurol. 300, 5–25 (1990)

    Article  CAS  Google Scholar 

  17. McAnany, J. J. & Levine, M. W. Magnocellular and parvocellular visual pathway contributions to visual field anisotropies. Vision Res. 47, 2327–2336 (2007)

    Article  Google Scholar 

  18. Cowey, A., Stoerig, P. & Perry, V. H. Transneuronal retrograde degeneration of retinal ganglion cells after damage to striate cortex in macaque monkeys: selective loss of Pβ cells. Neuroscience 29, 65–80 (1989)

    Article  CAS  Google Scholar 

  19. Diamond, I. T. & Hall, W. C. Evolution of neocortex. Science 164, 251–262 (1969)

    Article  ADS  CAS  Google Scholar 

  20. Mohler, C. W. & Wurtz, R. H. Role of striate cortex and superior colliculus in visual guidance of saccadic eye movements in monkeys. J. Neurophysiol. 40, 74–94 (1977)

    Article  CAS  Google Scholar 

  21. Rodman, H. R., Gross, C. G. & Albright, T. D. Afferent basis of visual response properties in area MT of the macaque. II. Effects of superior colliculus removal. J. Neurosci. 10, 1154–1164 (1990)

    Article  CAS  Google Scholar 

  22. Stepniewska, I., Qi, H. X. & Kaas, J. H. Do superior colliculus projection zones in the inferior pulvinar project to MT in primates? Eur. J. Neurosci. 11, 469–480 (1999)

    Article  CAS  Google Scholar 

  23. Berman, R. A. & Wurtz, R. H. Functional identification of a pulvinar path from superior colliculus to cortical area MT. J. Neurosci 30, 6342–6354 (2010)

    Article  CAS  Google Scholar 

  24. Lyon, D. C., Nassi, J. J. & Callaway, E. M. A disynaptic relay from superior colliculus to dorsal stream visual cortex in macaque monkey. Neuron 65, 270–279 (2010)

    Article  CAS  Google Scholar 

  25. Bender, D. B. Visual activation of neurons in the primate pulvinar depends on cortex but not colliculus. Brain Res. 279, 258–261 (1983)

    Article  CAS  Google Scholar 

  26. Schiller, P. H., Logothetis, N. K. & Charles, E. R. Functions of the colour-opponent and broad-band channels of the visual system. Nature 343, 68–70 (1990)

    Article  ADS  CAS  Google Scholar 

  27. Maunsell, J. H., Nealey, T. A. & DePriest, D. D. Magnocellular and parvocellular contributions to responses in the middle temporal visual area (MT) of the macaque monkey. J. Neurosci. 10, 3323–3334 (1990)

    Article  CAS  Google Scholar 

  28. Cowey, A. & Stoerig, P. Projection patterns of surviving neurons in the dorsal lateral geniculate nucleus following discrete lesions of striate cortex: implications for residual vision. Exp. Brain Res. 75, 631–638 (1989)

    Article  CAS  Google Scholar 

  29. Harting, J. K., Huerta, M. F., Hashikawa, T. & van Lieshout, D. P. Projection of the mammalian superior colliculus upon the dorsal lateral geniculate nucleus: organization of tectogeniculate pathways in nineteen species. J. Comp. Neurol. 304, 275–306 (1991)

    Article  CAS  Google Scholar 

  30. Bridge, H., Thomas, O., Jbabdi, S. & Cowey, A. Changes in connectivity after visual cortical brain damage underlie altered visual function. Brain 131, 1433–1444 (2008)

    Article  Google Scholar 

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Acknowledgements

We thank A. Maier and D. McMahon for comments on the manuscript; S. Smirnakis, R. Berman, R. Wurtz, B. Richmond, S. Guderian and M. Fukushima for discussions; C. Zhu and H. Merkle for magnetic resonance coil construction; K. Smith, N. Phipps, J. Yu, G. Dold, D. Ide and T. Talbot for technical assistance; D. Sheinberg for developing visual stimulation software; and members of the Brian Wandell laboratory for developing and sharing mrVista software. This work was supported by the Intramural Research Programme of the NIMH, the NINDS, and the NEI.

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Contributions

M.C.S. took the primary lead for all aspects of this work and wrote the paper; S.W.M. helped with experiments and analysis; J.T. helped with the experiments and developed the inactivation method; R.C.S. created the lesions; M.W. developed the inactivation method; A.J.P. helped with experiments and analysis; F.Q.Y. developed pre-processing software and optimized magnetic resonance sequences; and D.A.L. provided resources, acted in a supervisory role on all aspects of this work and wrote the paper.

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Correspondence to Michael C. Schmid.

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The authors declare no competing financial interests.

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Schmid, M., Mrowka, S., Turchi, J. et al. Blindsight depends on the lateral geniculate nucleus. Nature 466, 373–377 (2010). https://doi.org/10.1038/nature09179

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