Determinants of Global Color-Based Selection in Human Visual Cortex.

Feature attention operates in a spatially global way, with attended feature values being prioritized for selection outside the focus of attention. Accounts of global feature attention have emphasized feature competition as a determining factor. Here, we use magnetoencephalographic recordings in humans to test whether competition is critical for global feature selection to arise. Subjects performed a color/shape discrimination task in one visual field (VF), while irrelevant color probes were presented in the other unattended VF. Global effects of color attention were assessed by analyzing the response to the probe as a function of whether or not the probe's color was a target-defining color. We find that global color selection involves a sequence of modulations in extrastriate cortex, with an initial phase in higher tier areas (lateral occipital complex) followed by a later phase in lower tier retinotopic areas (V3/V4). Importantly, these modulations appeared with and without color competition in the focus of attention. Moreover, early parts of the modulation emerged for a task-relevant color not even present in the focus of attention. All modulations, however, were eliminated during simple onset-detection of the colored target. These results indicate that global color-based attention depends on target discrimination independent of feature competition in the focus of attention.

[1]  G. Boynton,et al.  Effects of feature-based attention on the motion aftereffect at remote locations , 2006, Vision Research.

[2]  S. Hillyard,et al.  Delayed Striate Cortical Activation during Spatial Attention , 2002, Neuron.

[3]  R. Desimone,et al.  Competitive Mechanisms Subserve Attention in Macaque Areas V2 and V4 , 1999, The Journal of Neuroscience.

[4]  R. Malach,et al.  Object-related activity revealed by functional magnetic resonance imaging in human occipital cortex. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[5]  Thomas G. Dietterich,et al.  Editors. Advances in Neural Information Processing Systems , 2002 .

[6]  J. Maunsell,et al.  Effects of Attention on the Processing of Motion in Macaque Middle Temporal and Medial Superior Temporal Visual Cortical Areas , 1999, The Journal of Neuroscience.

[7]  Kenji Kawano,et al.  Global and fine information coded by single neurons in the temporal visual cortex , 1999, Nature.

[8]  Alex R. Wade,et al.  Visual field maps and stimulus selectivity in human ventral occipital cortex , 2005, Nature Neuroscience.

[9]  John K. Tsotsos A Computational Perspective on Visual Attention , 2011 .

[10]  Christian M. Stoppel,et al.  Separable Mechanisms Underlying Global Feature-Based Attention , 2012, The Journal of Neuroscience.

[11]  N. Kanwisher,et al.  Stages of processing in face perception: an MEG study , 2002, Nature Neuroscience.

[12]  G. Boynton,et al.  Feature-Based Attentional Modulations in the Absence of Direct Visual Stimulation , 2007, Neuron.

[13]  C. Schroeder,et al.  Intermodal selective attention in monkeys. I: distribution and timing of effects across visual areas. , 2000, Cerebral cortex.

[14]  F. Hamker,et al.  Attention Alters Feature Space in Motion Processing , 2010, The Journal of Neuroscience.

[15]  S. Luck,et al.  Feature-based attention modulates feedforward visual processing , 2009, Nature Neuroscience.

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

[17]  Hans-Jochen Heinze,et al.  Object-based attention involves the sequential activation of feature-specific cortical modules , 2014, Nature Neuroscience.

[18]  Vincent Di Lollo,et al.  Electrophysiological Indices of Target and Distractor Processing in Visual Search , 2009, Journal of Cognitive Neuroscience.

[19]  D. Guthrie,et al.  Significance testing of difference potentials. , 1991, Psychophysiology.

[20]  Joshua B. Ewen,et al.  Inhibition Drives Early Feature-Based Attention , 2014, Psychological science.

[21]  J Duncan,et al.  Responses of neurons in macaque area V4 during memory-guided visual search. , 2001, Cerebral cortex.

[22]  Steven A. Hillyard,et al.  Global Facilitation of Attended Features Is Obligatory and Restricts Divided Attention , 2013, The Journal of Neuroscience.

[23]  Joonyeol Lee,et al.  Attentional Modulation of MT Neurons with Single or Multiple Stimuli in Their Receptive Fields , 2010, The Journal of Neuroscience.

[24]  Robert Desimone,et al.  Parallel and Serial Neural Mechanisms for Visual Search in Macaque Area V4 , 2005, Science.

[25]  Steven J Luck,et al.  Active suppression of distractors that match the contents of visual working memory , 2011, Visual cognition.

[26]  C. N. Boehler,et al.  Spatiotemporal Dynamics of Feature-Based Attention Spread: Evidence from Combined Electroencephalographic and Magnetoencephalographic Recordings , 2012, The Journal of Neuroscience.

[27]  J. Braun,et al.  Feature-based attention spreads preferentially in an object-specific manner , 2012, Vision Research.

[28]  D. Melcher,et al.  Implicit Attentional Selection of Bound Visual Features , 2005, Neuron.

[29]  J. Hegdé,et al.  Temporal dynamics of shape analysis in macaque visual area V2. , 2004, Journal of neurophysiology.

[30]  John H. R. Maunsell,et al.  Feature-based attention in visual cortex , 2006, Trends in Neurosciences.

[31]  J. Hegdé,et al.  Temporal dynamics of 2D and 3D shape representation in macaque visual area V4 , 2006, Visual Neuroscience.

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

[33]  S. Ullman Object recognition and segmentation by a fragment-based hierarchy , 2007, Trends in Cognitive Sciences.

[34]  Søren K. Andersen,et al.  Effects of Feature-selective and Spatial Attention at Different Stages of Visual Processing , 2011, Journal of Cognitive Neuroscience.

[35]  H. Komatsu,et al.  Effects of task demands on the responses of color-selective neurons in the inferior temporal cortex , 2007, Nature Neuroscience.

[36]  G. Boynton,et al.  Global effects of feature-based attention in human visual cortex , 2002, Nature Neuroscience.

[37]  K. Grill-Spector,et al.  The human visual cortex. , 2004, Annual review of neuroscience.

[38]  R. Desimone,et al.  Neural mechanisms of spatial selective attention in areas V1, V2, and V4 of macaque visual cortex. , 1997, Journal of neurophysiology.

[39]  Stefan Treue,et al.  Feature-based attention influences motion processing gain in macaque visual cortex , 1999, Nature.

[40]  J. Hegdé Time course of visual perception: Coarse-to-fine processing and beyond , 2008, Progress in Neurobiology.

[41]  S. Luck,et al.  Attention to Features Precedes Attention to Locations in Visual Search: Evidence from Electromagnetic Brain Responses in Humans , 2004, The Journal of Neuroscience.

[42]  Taosheng Liu,et al.  Constant spread of feature-based attention across the visual field , 2011, Vision Research.

[43]  Carsten Nicolas Boehler,et al.  Object-based Selection of Irrelevant Features Is Not Confined to the Attended Object , 2011, Journal of Cognitive Neuroscience.

[44]  B. Wandell,et al.  Visual Field Maps in Human Cortex , 2007, Neuron.

[45]  R. Desimone,et al.  Selective attention gates visual processing in the extrastriate cortex. , 1985, Science.

[46]  M. Fuchs,et al.  Linear and nonlinear current density reconstructions. , 1999, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[47]  Samuel J. Williamson,et al.  Advances in Biomagnetism , 1990, Springer US.

[48]  Diane M. Beck,et al.  Task-relevant and Task-irrelevant Dimensions Are Modulated Independently at a Task-irrelevant Location , 2012, Journal of Cognitive Neuroscience.

[49]  John K. Tsotsos,et al.  The center-surround profile of the focus of attention arises from recurrent processing in visual cortex. , 2009, Cerebral cortex.

[50]  John H. R. Maunsell,et al.  Attention to both space and feature modulates neuronal responses in macaque area V4. , 2000, Journal of neurophysiology.

[51]  R. Desimone,et al.  A backward progression of attentional effects in the ventral stream , 2009, Proceedings of the National Academy of Sciences.

[52]  S. C. Chong,et al.  Cross-feature spread of global attentional modulation in human area MT+ , 2005, Neuroreport.

[53]  Steven L Franconeri,et al.  Common-Fate Grouping as Feature Selection , 2011, Psychological science.

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

[55]  Matthias M. Müller,et al.  Color-selective attention need not be mediated by spatial attention. , 2009, Journal of vision.

[56]  Doris Y. Tsao,et al.  Neuroimaging Weighs In: Humans Meet Macaques in “Primate” Visual Cortex , 2003, The Journal of Neuroscience.

[57]  S. Treue,et al.  Feature-Based Attention Increases the Selectivity of Population Responses in Primate Visual Cortex , 2004, Current Biology.

[58]  G. Rhodes,et al.  Sex-specific norms code face identity. , 2011, Journal of vision.

[59]  G. Glover,et al.  Retinotopic organization in human visual cortex and the spatial precision of functional MRI. , 1997, Cerebral cortex.

[60]  R. Desimone,et al.  Responses of Neurons in Inferior Temporal Cortex during Memory- Guided Visual Search , 1998 .

[61]  S. Yamane,et al.  Population dynamics of face-responsive neurons in the inferior temporal cortex. , 2005, Cerebral cortex.

[62]  Chi-Hung Juan,et al.  Feedback to V1: a reverse hierarchy in vision , 2003, Experimental Brain Research.

[63]  Taosheng Liu,et al.  Global feature-based attention to orientation. , 2011, Journal of vision.

[64]  Steven J Luck,et al.  Capture versus suppression of attention by salient singletons: Electrophysiological evidence for an automatic attend-to-me signal , 2010, Attention, perception & psychophysics.

[65]  G. Boynton,et al.  Global feature-based attention for motion and color , 2003, Vision Research.

[66]  N. Kanwisher,et al.  Cortical Regions Involved in Perceiving Object Shape , 2000, The Journal of Neuroscience.

[67]  Stephen E. Robinson Environmental Noise Cancellation for Biomagnetic Measurements , 1989 .

[68]  B. B. Lee,et al.  The physiological basis of heterochromatic flicker photometry demonstrated in the ganglion cells of the macaque retina. , 1988, The Journal of physiology.

[69]  Takeo Watanabe,et al.  Perceptual learning rules based on reinforcers and attention , 2010, Trends in Cognitive Sciences.

[70]  G. Patricelli,et al.  Sexual selection: Male displays adjusted to female's response , 2002, Nature.

[71]  L. Busse,et al.  Attention to the Color of a Moving Stimulus Modulates Motion-Signal Processing in Macaque Area MT: Evidence for a Unified Attentional System , 2009, Front. Syst. Neurosci..

[72]  Alex L. White,et al.  Feature-based attention involuntarily and simultaneously improves visual performance across locations. , 2011, Journal of vision.

[73]  Tzyy-Ping Jung,et al.  Independent Component Analysis of Electroencephalographic Data , 1995, NIPS.

[74]  J-M Hopf,et al.  Dynamics of feature binding during object-selective attention , 2003, Proceedings of the National Academy of Sciences of the United States of America.