Orientation-selective chromatic mechanisms in human visual cortex.

We used functional magnetic resonance imaging (fMRI) at 3T in human participants to trace the chromatic selectivity of orientation processing through functionally defined regions of visual cortex. Our aim was to identify mechanisms that respond to chromatically defined orientation and to establish whether they are tuned specifically to color or operate in an essentially cue-invariant manner. Using an annular test region surrounded inside and out by an inducing stimulus, we found evidence of sensitivity to orientation defined by red-green (L-M) or blue-yellow (S-cone isolating) chromatic modulations across retinotopic visual cortex and of joint selectivity for color and orientation. The likely mechanisms underlying this selectivity are discussed in terms of orientation-specific lateral interactions and spatial summation within the receptive field.

[1]  Andrew T. Smith,et al.  Surround modulation measured with functional MRI in the human visual cortex. , 2003, Journal of neurophysiology.

[2]  S. Zeki Functional specialisation in the visual cortex of the rhesus monkey , 1978, Nature.

[3]  Brian A. Wandell,et al.  Population receptive field estimates in human visual cortex , 2008, NeuroImage.

[4]  Branka Spehar,et al.  Orientation-specific contextual modulation of the fMRI BOLD response to luminance and chromatic gratings in human visual cortex , 2009, Vision Research.

[5]  S. Kastner,et al.  Stimulus context modulates competition in human extrastriate cortex , 2005, Nature Neuroscience.

[6]  David J Heeger,et al.  Response Suppression in V1 Agrees with Psychophysics of Surround Masking , 2003, The Journal of Neuroscience.

[7]  P. Lennie,et al.  Chromatic mechanisms in lateral geniculate nucleus of macaque. , 1984, The Journal of physiology.

[8]  R Over,et al.  Colour selectivity in orientation masking and aftereffect. , 1973, Vision research.

[9]  A. Angelucci,et al.  Contribution of feedforward, lateral and feedback connections to the classical receptive field center and extra-classical receptive field surround of primate V1 neurons. , 2006, Progress in brain research.

[10]  R Perez,et al.  Neural mechanisms underlying stereoscopic vision , 1998, Progress in Neurobiology.

[11]  Wim Vanduffel,et al.  The Radial Bias: A Different Slant on Visual Orientation Sensitivity in Human and Nonhuman Primates , 2006, Neuron.

[12]  F. Tong,et al.  Decoding the visual and subjective contents of the human brain , 2005, Nature Neuroscience.

[13]  D. Ringach,et al.  The Operating Point of the Cortex: Neurons as Large Deviation Detectors , 2007, The Journal of Neuroscience.

[14]  J. B. Levitt,et al.  Functional properties of neurons in macaque area V3. , 1997, Journal of neurophysiology.

[15]  R. Shapley,et al.  The spatial transformation of color in the primary visual cortex of the macaque monkey , 2001, Nature Neuroscience.

[16]  K R Gegenfurtner,et al.  Processing of color, form, and motion in macaque area V2 , 1996, Visual Neuroscience.

[17]  K. Nakayama,et al.  Subjective contours, tilt aftereffects, and visual cortical organization , 1989, Vision Research.

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

[19]  D G Pelli,et al.  The VideoToolbox software for visual psychophysics: transforming numbers into movies. , 1997, Spatial vision.

[20]  P. Dayan,et al.  Space and time in visual context , 2007, Nature Reviews Neuroscience.

[21]  Andreas Bartels,et al.  Coding and binding of color and form in visual cortex. , 2010, Cerebral cortex.

[22]  M Coltheart,et al.  Letter: Colour-specificity and monocularity in the visual cortex. , 1973, Vision research.

[23]  P. Cavanagh,et al.  A minimum motion technique for judging equiluminance , 1983 .

[24]  Guido Gerig,et al.  User-guided 3D active contour segmentation of anatomical structures: Significantly improved efficiency and reliability , 2006, NeuroImage.

[25]  Geraint Rees,et al.  Combined orientation and colour information in human V1 for both L–M and S-cone chromatic axes , 2008, NeuroImage.

[26]  Patrick Cavanagh,et al.  Independent orientation-selective mechanisms for the cardinal directions of colour space , 1990, Vision Research.

[27]  C. McCollough Color Adaptation of Edge-Detectors in the Human Visual System , 1965, Science.

[28]  José V. Manjón,et al.  A nonparametric MRI inhomogeneity correction method , 2007, Medical Image Anal..

[29]  D. Hubel,et al.  Segregation of form, color, movement, and depth: anatomy, physiology, and perception. , 1988, Science.

[30]  G. Rees,et al.  Predicting the orientation of invisible stimuli from activity in human primary visual cortex , 2005, Nature Neuroscience.

[31]  Stephen A Engel,et al.  Adaptation of Oriented and Unoriented Color-Selective Neurons in Human Visual Areas , 2005, Neuron.

[32]  S. Kastner,et al.  Stimulus similarity modulates competitive interactions in human visual cortex. , 2007, Journal of vision.

[33]  Andreas Bartels,et al.  fMRI and its interpretations: an illustration on directional selectivity in area V5/MT , 2008, Trends in Neurosciences.

[34]  J. Gallant,et al.  Identifying natural images from human brain activity , 2008, Nature.

[35]  Branka Spehar,et al.  Colour and luminance selectivity of spatial and temporal interactions in orientation perception , 2003, Vision Research.

[36]  A. Stockman,et al.  The spectral sensitivities of the middle- and long-wavelength-sensitive cones derived from measurements in observers of known genotype , 2000, Vision Research.

[37]  D. Heeger,et al.  Two Retinotopic Visual Areas in Human Lateral Occipital Cortex , 2006, The Journal of Neuroscience.

[38]  Trichur Raman Vidyasagar Orientation specific colour adaptation at a binocular site , 1976, Nature.

[39]  J. Gibson,et al.  ADAPTATION , AFTEREFFECT AND CONTRAST IN THE PERCEPTION OF TILTED LINES , 2004 .

[40]  R. Rafal,et al.  Interactions between color and word processing in a flanker task. , 1999, Journal of experimental psychology. Human perception and performance.

[41]  D. J. Felleman,et al.  Distributed hierarchical processing in the primate cerebral cortex. , 1991, Cerebral cortex.

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

[43]  A. Leventhal,et al.  Concomitant sensitivity to orientation, direction, and color of cells in layers 2, 3, and 4 of monkey striate cortex , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[44]  D H Brainard,et al.  The Psychophysics Toolbox. , 1997, Spatial vision.

[45]  Colin W G Clifford,et al.  Interactions between color and luminance in the perception of orientation. , 2003, Journal of vision.

[46]  P. Lennie,et al.  Chromatic mechanisms in striate cortex of macaque , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[47]  Colin W.G. Clifford,et al.  Inter-ocular transfer of the tilt illusion shows that monocular orientation mechanisms are colour selective , 2005, Vision Research.

[48]  B J Richmond,et al.  Concurrent processing and complexity of temporally encoded neuronal messages in visual perception. , 1991, Science.

[49]  D. Mackay,et al.  Orientation-sensitive After-effects of Dichoptically Presented Colour and Form , 1973, Nature.

[50]  R. Shapley,et al.  The Orientation Selectivity of Color-Responsive Neurons in Macaque V1 , 2008, The Journal of Neuroscience.

[51]  D. G. Albrecht,et al.  Spatial mapping of monkey VI cells with pure color and luminance stimuli , 1984, Vision Research.

[52]  Leslie G. Ungerleider,et al.  Modulation of sensory suppression: implications for receptive field sizes in the human visual cortex. , 2001, Journal of neurophysiology.

[53]  B. Spehar,et al.  The Foveal Confluence in Human Visual Cortex , 2009, The Journal of Neuroscience.