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.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 51 print issues and online access
$199.00 per year
only $3.90 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
Change history
15 July 2009
A small correction was made to the Fig. 2 legend.
References
Weiskrantz, L., Warrington, E. K. & Sanders, M. D. Visual capacity in the hemianopic field following a restricted occipital ablation. Brain 97, 709–728 (1974)
Cowey, A. & Stoerig, P. Blindsight in monkeys. Nature 373, 247–249 (1995)
Keating, E. G. Residual spatial vision in the monkey after removal of striate and preoccipital cortex. Brain Res. 187, 271–290 (1980)
Cowey, A. The blindsight saga. Exp. Brain Res. 200, 3–24 (2010)
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)
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)
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)
Cowey, A. & Stoerig, P. Visual detection in monkeys with blindsight. Neuropsychologia 35, 929–939 (1997)
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)
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)
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)
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)
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)
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)
Cope, D. W., Hughes, S. W. & Crunelli, V. GABAA receptor-mediated tonic inhibition in thalamic neurons. J. Neurosci. 25, 11553–11563 (2005)
Curcio, C. A. & Allen, K. A. Topography of ganglion cells in human retina. J. Comp. Neurol. 300, 5–25 (1990)
McAnany, J. J. & Levine, M. W. Magnocellular and parvocellular visual pathway contributions to visual field anisotropies. Vision Res. 47, 2327–2336 (2007)
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)
Diamond, I. T. & Hall, W. C. Evolution of neocortex. Science 164, 251–262 (1969)
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)
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)
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)
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)
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)
Bender, D. B. Visual activation of neurons in the primate pulvinar depends on cortex but not colliculus. Brain Res. 279, 258–261 (1983)
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)
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)
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)
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)
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)
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.
Author information
Authors and Affiliations
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.
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing financial interests.
Supplementary information
Supplementary Information
This file contains Supplementary Figures 1-6 with legends, Supplementary Methods and References. (PDF 2166 kb)
Rights and permissions
About this article
Cite this article
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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/nature09179
This article is cited by
-
A clinico-anatomical dissection of the magnocellular and parvocellular pathways in a patient with the Riddoch syndrome
Brain Structure and Function (2024)
-
Does the Emotional Modulation of Visual Experience Entail the Cognitive Penetrability of Early Vision?
Review of Philosophy and Psychology (2023)
-
Conducting Channels in the Visual System. The Third Channel
Neuroscience and Behavioral Physiology (2022)
-
The posterior parietal cortex contributes to visuomotor processing for saccades in blindsight macaques
Communications Biology (2021)
-
Mouse visual cortex contains a region of enhanced spatial resolution
Nature Communications (2021)
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.