The primate visual system is believed to comprise two main pathways: a ventral pathway for conscious perception and a dorsal pathway that can process visual information and guide action without accompanying conscious knowledge. Evidence for this theory has come primarily from studies of neurological patients and animals. Using fMRI, we show here that even though observers are completely unaware of test object images owing to interocular suppression, their dorsal cortical areas demonstrate substantial activity for different types of visual objects, with stronger responses to images of tools than of human faces. This result also suggests that in binocular rivalry, substantial information in the suppressed eye can escape the interocular suppression and reach dorsal cortex.
This is a preview of subscription content, access via your institution
Open Access articles citing this article.
Scientific Reports Open Access 13 July 2022
Scientific Reports Open Access 07 June 2021
Experimental Brain Research Open Access 17 April 2021
Subscribe to Journal
Get full journal access for 1 year
only $6.58 per issue
All prices are NET prices.
VAT will be added later in the checkout.
Tax calculation will be finalised during checkout.
Get time limited or full article access on ReadCube.
All prices are NET prices.
Ungerleider, L.G. & Mishkin, M. Two cortical visual systems. in Analysis of Visual Behavior (eds. Ingle, D.J., Goodale, M.A. & Mansfield, R.J.W.) 549–586 (MIT Press, Cambridge, Massachusetts, 1982).
Milner, A.D. & Goodale, M.A. The Visual Brain in Action (Oxford University Press, Oxford, 1995).
James, T.W., Culham, J., Humphrey, G.K., Milner, A.D. & Goodale, M.A. Ventral occipital lesions impair object recognition but not object directed grasping: an fMRI study. Brain 126, 2463–2475 (2003).
Goodale, M.A., Milner, A.D., Jakobson, L.S. & Carey, D.P. A neurological dissociation between perceiving objects and grasping them. Nature 349, 154–156 (1991).
Kluver, H. & Bucy, P.C. An analysis of certain effects of bilateral temporal lobectomy in the rhesus monkey, with special reference to 'psychic blindness'. J. Psychol. 5, 33–54 (1938).
Goodale, M.A. & Westwood, D.A. An evolving view of duplex vision: separate but interacting cortical pathways for perception and action. Curr. Opin. Neurobiol. 14, 203–211 (2004).
Grill-Spector, K., Kourtzi, Z. & Kanwisher, N. The lateral occipital complex and its role in object recogntion. Vision Res. 41, 1409–1422 (2001).
Grill-Spector, K., Kushnir, T., Edelman, S., Itzchak, Y. & Malach, R. Cue-invariant activation in object-related areas of the human occipital lobe. Neuron 21, 191–202 (1998).
Dale, A.M. et al. Dynamic statistical parametric mapping: combining fMRI and MEG for high-resolution imaging of cortical activity. Neuron 26, 55–67 (2000).
Grill-Spector, K., Kushnir, T., Hendler, T. & Malach, R. The dynamics of object-selective activation correlate with recognition performance in humans. Nat. Neurosci. 3, 837–843 (2000).
James, T.W., Humphrey, G.K., Gati, J.S., Menon, R.S. & Goodale, M.A. The effects of visual object priming on brain activation before and after recognition. Curr. Biol. 10, 1017–1024 (2000).
James, T.W., Humphrey, G.K., Gati, J.S., Menon, R.S. & Goodale, M.A. Differential effects of viewpoint on object-driven activation in dorsal and ventral streams. Neuron 35, 793–801 (2002).
Murray, S.O., Olshausen, B.A. & Woods, D.L. Processing shape, motion and three-dimensional shape-from-motion in the human cortex. Cereb. Cortex 13, 508–516 (2003).
Chao, L.L. & Martin, A. Representation of manipulable man-made objects in the dorsal stream. Neuroimage 12, 478–484 (2000).
Tong, F., Nakayama, K., Vaughan, J.T. & Kanwisher, N. Binocular rivalry and visual awareness in human extrastriate cortex. Neuron 21, 753–759 (1998).
Bar, M. et al. Cortical mechanisms specific to explicit visual object recognition. Neuron 29, 529–535 (2001).
Sheinberg, D.L. & Logothetis, N.K. The role of temporal cortical areas in perceptual organization. Proc. Natl. Acad. Sci. USA 94, 3408–3413 (1997).
Breese, B.B. Binocular rivalry. Psychol. Rev. 16, 410–415 (1909).
Blake, R. Primer on binocular rivalry, including controversial issues. Brain Mind 2, 5–38 (2001).
Williams, M.A., Morris, A.P., McGlone, F., Abbott, D.F. & Mattingley, J.B. Amygdala responses to fearful and happy facial expressions under conditions of binocular suppression. J. Neurosci. 24, 2898–2904 (2004).
Pasley, B.N., Mayes, L.C. & Schultz, R.T. Subcortical discrimination of unperceived objects during binocular rivalry. Neuron 42, 163–172 (2004).
Kanwisher, N., Downing, P., Epstein, R. & Kourtzi, Z. Functional neuroimaging of human visual recognition. in The Handbook of Functional Neuroimaging of Cognition (eds. Cabeza, R. & Kingstone, A.) 109–152 (MIT Press, Cambridge, Massachusetts, 2001).
Claeys, K.G., Lindsey, D.T., De Schutter, E. & Orban, G.A. A higher order motion region in human inferior parietal lobule: evidence from fMRI. Neuron 40, 631–642 (2003).
Lee, S.H., Blake, R. & Heeger, D.J. Traveling waves of activity in primary visual cortex during binocular rivalry. Nat. Neurosci. 8, 22–23 (2005).
Lee, S.H. & Blake, R. V1 activity is reduced during binocular rivalry. J. Vis. 2, 618–26 (2002).
Polonsky, A., Blake, R., Braun, J. & Heeger, D.J. Neuronal activity in human primary visual cortex correlates with perception during binocular rivalry. Nat. Neurosci. 3, 1153–1159 (2000).
Weiskrantz, L. Consciousness Lost and Found (Oxford University Press, Oxford, 1997).
Sincich, L.C., Park, K.F., Wohlgenuth, M.J. & Horton, J.C. Bypassing V1: a direct geniculate input to area MT. Nat. Neurosci. 7, 1123–1128 (2004).
He, S., Carlson, T.A. & Chen, X. Parallel pathways and temporal dynamics in binocular rivalry. in Binocular Rivalry and Perceptual Ambiguity (eds. Alais, D. & Blake, R.) (MIT Press, Cambridge, Massachusetts, 2005).
Livingstone, M.S. & Hubel, D.H. Psychophysical evidence for separate channels for the perception of form, color, movement, and depth. J. Neurosci. 7, 3416–3468 (1987).
Logothetis, N.K. & Schall, J.D. Neuronal correlates of subjective visual perception. Science 245, 761–763 (1989).
Sereno, M.I. et al. Borders of multiple visual areas in humans revealed by functional magnetic resonance imaging. Science 268, 889–893 (1995).
Engel, S.A., Glover, G.H. & Wandell, B.A. Retinotopic organization in human visual cortex and the spatial precision of functional MRI. Cereb. Cortex 7, 181–192 (1997).
Talairach, J. & Tournoux, P. Co-Planar Stereotaxic Atlas of the Human Brain (Thieme, New York, 1988).
We thank S. Murray, S. Cheung and Y. Jiang for their technical assistance and P. Costello for help with the manuscript. This research was supported by the James S. McDonnell foundation, the US National Institutes of Health and the University of Minnesota's Eva O. Miller Fellowship and Graduate Research Partnership Program Award.
The authors declare no competing financial interests.
About this article
Cite this article
Fang, F., He, S. Cortical responses to invisible objects in the human dorsal and ventral pathways. Nat Neurosci 8, 1380–1385 (2005). https://doi.org/10.1038/nn1537
This article is cited by
Scientific Reports (2022)
Informative neural representations of unseen contents during higher-order processing in human brains and deep artificial networks
Nature Human Behaviour (2022)
Current Psychology (2022)
Brain Structure and Function (2022)