Early correlates of visual awareness in the human brain: Time and place from event-related brain potentials.

When something appears, how soon is the first neural correlate of awareness of it, and where is that activity in the brain? To answer these questions, we measured the electroencephalogram under conditions in which visual stimuli changed identically but in which awareness differed. We manipulated awareness by using binocular rivalry between orthogonal gratings viewed one to each eye. Then we changed the orientation of the grating to one eye to be the same as that to the other eye. Because of the rivalry, sometimes this happened to the visible grating, producing a clear change in perceived orientation, and other times it happened to the invisible grating, producing no change in perceived orientation. This procedure allowed us to analyze time-locked topographic scalp and tomographic primary current densities of the event-related potentials to physically identical events differing in their perceptual consequences. When the change in orientation reached awareness, neural responses began at about 100 ms, spreading mainly from dorsal occipital areas. When the change in orientation did not reach awareness, neural responses also began at about 100 ms, but they were attenuated, particularly in the right fusiform gyrus. We place the earliest correlate of visual awareness following binocular rivalry in the ventrolateral occipitotemporal cortex.

[1]  Delphine Pins,et al.  The neural correlates of conscious vision. , 2003, Cerebral cortex.

[2]  M. Goodale,et al.  Separate visual pathways for perception and action , 1992, Trends in Neurosciences.

[3]  Sabine Kastner,et al.  Neural correlates of binocular rivalry in the human lateral geniculate nucleus , 2005, Nature Neuroscience.

[4]  Terry M. Peters,et al.  3D statistical neuroanatomical models from 305 MRI volumes , 1993, 1993 IEEE Conference Record Nuclear Science Symposium and Medical Imaging Conference.

[5]  John C. Marshall,et al.  Sight unseen? , 1992, Current Biology.

[6]  F. Valle-Inclán,et al.  Electrical activity in primary visual area due to interocular suppression , 2001, Neuroreport.

[7]  Charles Wheatstone,et al.  Contributions to the Physiology of Vision. , 1837 .

[8]  T. Allison,et al.  Face-Specific Processing in the Human Fusiform Gyrus , 1997, Journal of Cognitive Neuroscience.

[9]  R. Deichmann,et al.  Eye-specific effects of binocular rivalry in the human lateral geniculate nucleus , 2005, Nature.

[10]  A. Milner,et al.  Cerebral correlates of visual awareness , 1995, Neuropsychologia.

[11]  S. Hochstein,et al.  View from the Top Hierarchies and Reverse Hierarchies in the Visual System , 2002, Neuron.

[12]  A. Dale,et al.  Functional Analysis of V3A and Related Areas in Human Visual Cortex , 1997, The Journal of Neuroscience.

[13]  N. Trujillo-Barreto,et al.  3D Statistical Parametric Mapping of EEG Source Spectra by Means of Variable Resolution Electromagnetic Tomography (VARETA) , 2001, Clinical EEG.

[14]  C. Wheatstone Contributions to the physiology of vision.—Part II.—On some remarkable, and hitherto unobserved, phenomena of binocular vision. A Bakerian lecture , 1852 .

[15]  Nelson J. Trujillo-Barreto,et al.  Bayesian model averaging in EEG/MEG imaging , 2004, NeuroImage.

[16]  M. Scherg,et al.  Intracerebral Sources of Human Auditory-Evoked Potentials , 1999, Audiology and Neurotology.

[17]  Stephen A. Engel,et al.  Interocular rivalry revealed in the human cortical blind-spot representation , 2001, Nature.

[18]  F. Perrin,et al.  Spherical splines for scalp potential and current density mapping. , 1989, Electroencephalography and clinical neurophysiology.

[19]  C Kaernbach,et al.  Effects of consciousness on human brain waves following binocular rivalry. , 1999, Neuroreport.

[20]  Michael Bach,et al.  Bistable perception -- along the processing chain from ambiguous visual input to a stable percept. , 2006, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[21]  K. Nakayama,et al.  Binocular Rivalry and Visual Awareness in Human Extrastriate Cortex , 1998, Neuron.

[22]  A. Dale,et al.  New images from human visual cortex , 1996, Trends in Neurosciences.

[23]  Margot J. Taylor,et al.  Guidelines for using human event-related potentials to study cognition: recording standards and publication criteria. , 2000, Psychophysiology.

[24]  V. Lamme,et al.  The distinct modes of vision offered by feedforward and recurrent processing , 2000, Trends in Neurosciences.

[25]  E. Schröger,et al.  Binocular rivalry is partly resolved at early processing stages with steady and with flickering presentation: a human event-related brain potential study , 2004, Neuroscience Letters.

[26]  R. Blake © 2001 Kluwer Academic Publishers. Printed in the Netherlands. 5 A Primer on Binocular Rivalry, Including Current Controversies , 2000 .

[27]  W. Singer,et al.  Temporal binding and the neural correlates of sensory awareness , 2001, Trends in Cognitive Sciences.

[28]  F. Donders On the speed of mental processes. , 1969, Acta psychologica.

[29]  M. Gazzaniga,et al.  Combined spatial and temporal imaging of brain activity during visual selective attention in humans , 1994, Nature.

[30]  Michael Bach,et al.  The Necker cube—an ambiguous figure disambiguated in early visual processing , 2005, Vision Research.

[31]  V. Lamme Why visual attention and awareness are different , 2003, Trends in Cognitive Sciences.

[32]  G. Mangun,et al.  Covariations in ERP and PET measures of spatial selective attention in human extrastriate visual cortex , 1997, Human brain mapping.

[33]  S A Hackley,et al.  Early visual processing during binocular rivalry studied with visual evoked potentials. , 1999, Neuroreport.

[34]  C. Wheatstone XVIII. Contributions to the physiology of vision. —Part the first. On some remarkable, and hitherto unobserved, phenomena of binocular vision , 1962, Philosophical Transactions of the Royal Society of London.

[35]  E. Vogel,et al.  Sensory gain control (amplification) as a mechanism of selective attention: electrophysiological and neuroimaging evidence. , 1998, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[36]  W J Levelt,et al.  Note on the distribution of dominance times in binocular rivalry. , 1967, British journal of psychology.

[37]  H. Spekreijse,et al.  Two distinct modes of sensory processing observed in monkey primary visual cortex (V1) , 2001, Nature Neuroscience.

[38]  Jane Redfern Jones,et al.  View at the top. , 2007, Nursing standard (Royal College of Nursing (Great Britain) : 1987).

[39]  Geraint Rees,et al.  Neuroimaging of visual awareness in patients and normal subjects , 2001, Current Opinion in Neurobiology.

[40]  S. Hillyard,et al.  Cortical sources of the early components of the visual evoked potential , 2002, Human brain mapping.

[41]  Jacob Moleschott Untersuchungen zur Naturlehre des Menschen und der Thiere , 1981 .

[42]  A. Norcia,et al.  A method for investigating binocular rivalry in real-time with the steady-state VEP , 1997, Vision Research.

[43]  P. Walker Stochastic properties of binocular rivalry alternations , 1975 .

[44]  Michael A. Pitts,et al.  Electrophysiological correlates of perceptual reversals for three different types of multistable images. , 2007, Journal of vision.

[45]  S. Hillyard,et al.  Involvement of striate and extrastriate visual cortical areas in spatial attention , 1999, Nature Neuroscience.

[46]  B. Julesz,et al.  Neurontropy, an entropy-like measure of neural correlation, in binocular fusion and rivalry , 1976, Biological Cybernetics.

[47]  B. Julesz,et al.  The neural transfer characteristic (neurontropy) for binocular stochastic stimulation , 2004, Biological Cybernetics.

[48]  Minna Lehtonen,et al.  Independence of visual awareness from the scope of attention: an electrophysiological study. , 2006, Cerebral cortex.

[49]  D. Heeger,et al.  Neuronal activity in human primary visual cortex correlates with perception during binocular rivalry , 2000, Nature Neuroscience.

[50]  P. Valdés-Sosa,et al.  Variable Resolution Electric-Magnetic Tomography , 2000 .

[51]  K. Zilles,et al.  The Neural Basis of Vertical and Horizontal Line Bisection Judgments: An fMRI Study of Normal Volunteers , 2001, NeuroImage.

[52]  Stephen L Macknik,et al.  Visibility, visual awareness, and visual masking of simple unattended targets are confined to areas in the occipital cortex beyond human V1/V2. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[53]  N. Logothetis,et al.  Activity changes in early visual cortex reflect monkeys' percepts during binocular rivalry , 1996, Nature.

[54]  Alan C. Evans,et al.  Searching scale space for activation in PET images , 1996, Human brain mapping.

[55]  G. Rees,et al.  Neural correlates of perceptual rivalry in the human brain. , 1998, Science.

[56]  Ramesh Srinivasan,et al.  MEG phase follows conscious perception during binocular rivalry induced by visual stream segregation. , 2006, Cerebral cortex.

[57]  D. P. Russell,et al.  Increased Synchronization of Neuromagnetic Responses during Conscious Perception , 1999, The Journal of Neuroscience.

[58]  C. Frith,et al.  Interhemispheric Differences in Extrastriate Areas during Visuo-Spatial Selective Attention , 2000, NeuroImage.

[59]  C. C. Wood,et al.  Scalp distributions of event-related potentials: an ambiguity associated with analysis of variance models. , 1985, Electroencephalography and clinical neurophysiology.