Predicting the orientation of invisible stimuli from activity in human primary visual cortex

Humans can experience aftereffects from oriented stimuli that are not consciously perceived, suggesting that such stimuli receive cortical processing. Determining the physiological substrate of such effects has proven elusive owing to the low spatial resolution of conventional human neuroimaging techniques compared to the size of orientation columns in visual cortex. Here we show that even at conventional resolutions it is possible to use fMRI to obtain a direct measure of orientation-selective processing in V1. We found that many parts of V1 show subtle but reproducible biases to oriented stimuli, and that we could accumulate this information across the whole of V1 using multivariate pattern recognition. Using this information, we could then successfully predict which one of two oriented stimuli a participant was viewing, even when masking rendered that stimulus invisible. Our findings show that conventional fMRI can be used to reveal feature-selective processing in human cortex, even for invisible stimuli.

[1]  David G. Stork,et al.  Pattern Classification , 1973 .

[2]  M. Yukie,et al.  Direct projection from the dorsal lateral geniculate nucleus to the prestriate cortex in macaque monkeys , 1981, The Journal of comparative neurology.

[3]  A. Grinvald,et al.  Relationships between orientation-preference pinwheels, cytochrome oxidase blobs, and ocular-dominance columns in primate striate cortex. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[4]  B. Everitt,et al.  Applied Multivariate Data Analysis. , 1993 .

[5]  K. Obermayer,et al.  Geometry of orientation and ocular dominance columns in monkey striate cortex , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[6]  Karl J. Friston,et al.  Statistical parametric maps in functional imaging: A general linear approach , 1994 .

[7]  J W Belliveau,et al.  Borders of multiple visual areas in humans revealed by functional magnetic resonance imaging. , 1995, Science.

[8]  C. Koch,et al.  Are we aware of neural activity in primary visual cortex? , 1995, Nature.

[9]  P. Cavanagh,et al.  Attentional resolution and the locus of visual awareness , 1996, Nature.

[10]  E. Vogel,et al.  Word meanings can be accessed but not reported during the attentional blink , 1996, Nature.

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

[12]  Guillermo Sapiro,et al.  Creating connected representations of cortical gray matter for functional MRI visualization , 1997, IEEE Transactions on Medical Imaging.

[13]  D. Snodderly,et al.  A Dissociation Between Brain Activity and Perception: Chromatically Opponent Cortical Neurons Signal Chromatic Flicker that is not Perceived , 1997, Vision Research.

[14]  M. Livingstone,et al.  Neuronal correlates of visibility and invisibility in the primate visual system , 1998, Nature Neuroscience.

[15]  Jean-Baptiste Poline,et al.  Inferring behavior from functional brain images , 1998, Nature Neuroscience.

[16]  S. Dehaene,et al.  Imaging unconscious semantic priming , 1998, Nature.

[17]  A. Dale,et al.  Functional analysis of primary visual cortex (V1) in humans. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[18]  Ravi S. Menon,et al.  An fMRI study of the selective activation of human extrastriate form vision areas by radial and concentric gratings , 2000, Current Biology.

[19]  C. Frith,et al.  Unconscious activation of visual cortex in the damaged right hemisphere of a parietal patient with extinction. , 2000, Brain : a journal of neurology.

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

[21]  B. Wandell,et al.  Visualization and Measurement of the Cortical Surface , 2000, Journal of Cognitive Neuroscience.

[22]  C. Furmanski,et al.  An oblique effect in human primary visual cortex , 2000, Nature Neuroscience.

[23]  R. Rafal,et al.  Neural fate of seen and unseen faces in visuospatial neglect: A combined event-related functional MRI and event-related potential study , 2001, Proceedings of the National Academy of Sciences of the United States of America.

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

[25]  Shigeo Abe DrEng.  Pattern Classification , 2001, Springer London.

[26]  Rainer Goebel,et al.  Sustained extrastriate cortical activation without visual awareness revealed by fMRI studies of hemianopic patients , 2001, Vision Research.

[27]  A. Ishai,et al.  Distributed and Overlapping Representations of Faces and Objects in Ventral Temporal Cortex , 2001, Science.

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

[29]  Sheng He,et al.  Orientation-selective adaptation and tilt after-effect from invisible patterns , 2001, Nature.

[30]  S Zeki,et al.  The relationship between cortical activation and perception investigated with invisible stimuli , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[31]  Eric R. Ziegel,et al.  Applied Multivariate Data Analysis , 2002, Technometrics.

[32]  T. Carlson,et al.  Patterns of Activity in the Categorical Representations of Objects , 2003, Journal of Cognitive Neuroscience.

[33]  G. Boynton,et al.  Orientation-Specific Adaptation in Human Visual Cortex , 2003, The Journal of Neuroscience.

[34]  Frank Tong,et al.  Cognitive neuroscience: Primary visual cortex and visual awareness , 2003, Nature Reviews Neuroscience.

[35]  David D. Cox,et al.  Functional magnetic resonance imaging (fMRI) “brain reading”: detecting and classifying distributed patterns of fMRI activity in human visual cortex , 2003, NeuroImage.

[36]  Gerald Westheimer,et al.  The distribution of preferred orientations in the peripheral visual field , 2003, Vision Research.

[37]  T. Carlson,et al.  Patterns of Activity in the Categorical Representations of Objects , 2003 .

[38]  David J. Heeger,et al.  Neuronal correlates of perception in early visual cortex , 2003, Nature Neuroscience.

[39]  Reza Rajimehr,et al.  Unconscious Orientation Processing , 2004, Neuron.

[40]  Deborah E. Hannula,et al.  Imaging implicit perception: promise and pitfalls , 2005, Nature Reviews Neuroscience.

[41]  Lorraine M. McDonnell,et al.  THE PROMISE AND THE PITFALLS , 2007 .

[42]  R. K. Simpson.  Nature Neuroscience , 2022 .