Color contrast adaptation: fMRI fails to predict behavioral adaptation

fMRI-adaptation is a valuable tool for inferring the selectivity of neural responses. Here we use it in human color vision to test the selectivity of responses to S-cone opponent (blue-yellow), L/M-cone opponent (red-green), and achromatic (Ach) contrast across nine regions of interest in visual cortex. We measure psychophysical adaptation, using comparable stimuli to the fMRI-adaptation, and find significant selective adaptation for all three stimulus types, implying separable visual responses to each. For fMRI-adaptation, we find robust adaptation but, surprisingly, much less selectivity due to high levels of cross-adaptation in all conditions. For all BY and Ach test/adaptor pairs, selectivity is absent across all ROIs. For RG/Ach stimulus pairs, this paradigm has previously shown selectivity for RG in ventral areas and for Ach in dorsal areas. For chromatic stimulus pairs (RG/BY), we find a trend for selectivity in ventral areas. In conclusion, we find an overall lack of correspondence between BOLD and behavioral adaptation suggesting they reflect different aspects of the underlying neural processes. For example, raised cross-stimulus adaptation in fMRI may reflect adaptation of the broadly-tuned normalization pool. Finally, we also identify a longer-timescale adaptation (1-h) in both BOLD and behavioral data. This is greater for chromatic than achromatic contrast. The longer-timescale BOLD effect was more evident in the higher ventral areas than in V1, consistent with increasing windows of temporal integration for higher-order areas.

[1]  A. Kleinschmidt,et al.  Temporal Tuning Properties along the Human Ventral Visual Stream , 2012, The Journal of Neuroscience.

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

[3]  Dorita H. F. Chang,et al.  The selectivity of responses to red‐green colour and achromatic contrast in the human visual cortex: an fMRI adaptation study , 2015, The European journal of neuroscience.

[4]  Justin L. Gardner,et al.  Contrast Adaptation and Representation in Human Early Visual Cortex , 2005, Neuron.

[5]  Rhea T. Eskew,et al.  Higher order color mechanisms: A critical review , 2009, Vision Research.

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

[7]  Bevil R. Conway,et al.  Color-tuned neurons are spatially clustered according to color preference within alert macaque posterior inferior temporal cortex , 2009, Proceedings of the National Academy of Sciences.

[8]  A Bradley,et al.  Failures of isoluminance caused by ocular chromatic aberrations. , 1992, Applied optics.

[9]  P. Lennie,et al.  Habituation Reveals Fundamental Chromatic Mechanisms in Striate Cortex of Macaque , 2008, The Journal of Neuroscience.

[10]  Adrian T. Lee,et al.  fMRI of human visual cortex , 1994, Nature.

[11]  Daniel Kersten,et al.  Spatially specific FMRI repetition effects in human visual cortex. , 2006, Journal of neurophysiology.

[12]  S. Thompson-Schill,et al.  Varying Timescales of Stimulus Integration Unite Neural Adaptation and Prototype Formation , 2016, Current Biology.

[13]  Brenna Argall,et al.  SUMA: an interface for surface-based intra- and inter-subject analysis with AFNI , 2004, 2004 2nd IEEE International Symposium on Biomedical Imaging: Nano to Macro (IEEE Cat No. 04EX821).

[14]  D. Heeger,et al.  A Hierarchy of Temporal Receptive Windows in Human Cortex , 2008, The Journal of Neuroscience.

[15]  D. Heeger,et al.  Categorical Clustering of the Neural Representation of Color , 2013, The Journal of Neuroscience.

[16]  John T. Serences,et al.  Attention modulates spatial priority maps in the human occipital, parietal and frontal cortices , 2013, Nature Neuroscience.

[17]  M. Webster,et al.  Changes in colour appearance following post-receptoral adaptation , 1991, Nature.

[18]  J. Movshon,et al.  Pattern adaptation and cross-orientation interactions in the primary visual cortex , 1998, Neuropharmacology.

[19]  Damien J. Mannion,et al.  Color responsiveness argues against a dorsal component of human V4. , 2011, Journal of vision.

[20]  Y. Benjamini,et al.  Controlling the false discovery rate: a practical and powerful approach to multiple testing , 1995 .

[21]  Nicolas P Cottaris,et al.  Artifacts in spatiochromatic stimuli due to variations in preretinal absorption and axial chromatic aberration: implications for color physiology. , 2003, Journal of the Optical Society of America. A, Optics, image science, and vision.

[22]  Gregory D Horwitz,et al.  V1 mechanisms underlying chromatic contrast detection. , 2013, Journal of neurophysiology.

[23]  D. Heeger,et al.  Retinotopy and Functional Subdivision of Human Areas MT and MST , 2002, The Journal of Neuroscience.

[24]  K. Gunther,et al.  Non-cardinal color mechanism strength differs across color planes but not across subjects. , 2014, Journal of the Optical Society of America. A, Optics, image science, and vision.

[25]  D. Hubel,et al.  Receptive fields of single neurones in the cat's striate cortex , 1959, The Journal of physiology.

[26]  E. DeYoe,et al.  Analysis and use of FMRI response delays , 2001, Human brain mapping.

[27]  R. Hess,et al.  Responses of the human visual cortex and LGN to achromatic and chromatic temporal modulations: an fMRI study. , 2010, Journal of vision.

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

[29]  Bevil R. Conway,et al.  Color-Biased Regions of the Ventral Visual Pathway Lie between Face- and Place-Selective Regions in Humans, as in Macaques , 2016, The Journal of Neuroscience.

[30]  Jonas Larsson,et al.  Spatial specificity and inheritance of adaptation in human visual cortex , 2015, Journal of neurophysiology.

[31]  R. Shapley,et al.  Color in the Cortex: single- and double-opponent cells , 2011, Vision Research.

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

[33]  M. Webster,et al.  The influence of contrast adaptation on color appearance , 1994, Vision Research.

[34]  Anders M. Dale,et al.  Cortical Surface-Based Analysis I. Segmentation and Surface Reconstruction , 1999, NeuroImage.

[35]  N. Logothetis What we can do and what we cannot do with fMRI , 2008, Nature.

[36]  Koji Inui,et al.  Temporal Dynamics of Neural Adaptation Effect in the Human Visual Ventral Stream , 2004, The Journal of Neuroscience.

[37]  Angela M. Brown,et al.  Higher order color mechanisms , 1986, Vision Research.

[38]  Michael A Webster,et al.  Dynamics of color contrast adaptation. , 2014, Journal of the Optical Society of America. A, Optics, image science, and vision.

[39]  R. Shapley,et al.  Cone inputs in macaque primary visual cortex. , 2004, Journal of Neurophysiology.

[40]  G. Boynton,et al.  Adaptation: from single cells to BOLD signals , 2006, Trends in Neurosciences.

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

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

[43]  Farshad Moradi,et al.  Adaptation of cerebral oxygen metabolism and blood flow and modulation of neurovascular coupling with prolonged stimulation in human visual cortex , 2013, NeuroImage.

[44]  D. W. Heeley,et al.  Cardinal directions of color space , 1982, Vision Research.

[45]  K. Mullen The contrast sensitivity of human colour vision to red‐green and blue‐yellow chromatic gratings. , 1985, The Journal of physiology.

[46]  Dorita H. F. Chang,et al.  Color responses and their adaptation in human superior colliculus and lateral geniculate nucleus , 2016, NeuroImage.

[47]  Kenichi Ueno,et al.  Hue Selectivity in Human Visual Cortex Revealed by Functional Magnetic Resonance Imaging , 2015, Cerebral cortex.

[48]  K. Mullen,et al.  Effect of overlaid luminance contrast on perceived color contrast: Shadows enhance, borders suppress. , 2016, Journal of vision.

[49]  Serge O Dumoulin,et al.  Color responses of the human lateral geniculate nucleus: selective amplification of S-cone signals between the lateral geniculate nucleno and primary visual cortex measured with high-field fMRI , 2008, The European journal of neuroscience.

[50]  A. Roe,et al.  Functional organization for color and orientation in macaque V4 , 2010, Nature Neuroscience.

[51]  Brian A Wandell,et al.  Visual field map clusters in human cortex , 2005, Philosophical Transactions of the Royal Society B: Biological Sciences.

[52]  T. Albright,et al.  Blue-yellow signals are enhanced by spatiotemporal luminance contrast in macaque V1. , 2005, Journal of neurophysiology.

[53]  Bevil R. Conway,et al.  Toward a Unified Theory of Visual Area V4 , 2012, Neuron.

[54]  R. Hess,et al.  Selectivity of human retinotopic visual cortex to S‐cone‐opponent, L/M‐cone‐opponent and achromatic stimulation , 2007, The European journal of neuroscience.

[55]  N. Logothetis,et al.  Integration of Local Features into Global Shapes Monkey and Human fMRI Studies , 2003, Neuron.

[56]  Janneke F. M. Jehee,et al.  Attention Improves Encoding of Task-Relevant Features in the Human Visual Cortex , 2011, The Journal of Neuroscience.

[57]  R W Cox,et al.  AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. , 1996, Computers and biomedical research, an international journal.

[58]  C. Furmanski,et al.  Selective Adaptation to Color Contrast in Human Primary Visual Cortex , 2001, The Journal of Neuroscience.

[59]  Kathy T. Mullen,et al.  S-cone contributions to linear and non-linear motion processing , 2007, Vision Research.

[60]  D. Kersten,et al.  Orientation-tuned FMRI adaptation in human visual cortex. , 2005, Journal of neurophysiology.