Object-based attention to one of two superimposed surfaces alters responses in human early visual cortex.

Faced with an overwhelming amount of sensory information, we are able to prioritize the processing of select spatial locations and visual features. The neuronal mechanisms underlying such spatial and feature-based selection have been studied in considerable detail. More recent work shows that attention can also be allocated to objects, even spatially superimposed objects composed of dynamically changing features that must be integrated to create a coherent object representation. Much less is known about the mechanisms underlying such object-based selection. Our goal was to investigate behavioral and neuronal responses when attention was directed to one of two objects, specifically one of two superimposed transparent surfaces, in a task designed to preclude space-based and feature-based selection. We used functional magnetic resonance imaging (fMRI) to measure changes in blood oxygen level-dependent (BOLD) signals when attention was deployed to one or the other surface. We found that visual areas V1, V2, V3, V3A, and MT+ showed enhanced BOLD responses to translations of an attended relative to an unattended surface. These results reveal that visual areas as early as V1 can be modulated by attending to objects, even objects defined by dynamically changing elements. This provides definitive evidence in humans that early visual areas are involved in a seemingly high-order process. Furthermore, our results suggest that these early visual areas may participate in object-specific feature "binding," a process that seemingly must occur for an object or a surface to be the unit of attentional selection.

[1]  Winrich A. Freiwald,et al.  Attention to Surfaces Modulates Motion Processing in Extrastriate Area MT , 2007, Neuron.

[2]  Pieter R. Roelfsema,et al.  Object-based attention in the primary visual cortex of the macaque monkey , 1998, Nature.

[3]  J. Reynolds,et al.  Exogenously cued attention triggers competitive selection of surfaces , 2003, Vision Research.

[4]  B. Efron Nonparametric estimates of standard error: The jackknife, the bootstrap and other methods , 1981 .

[5]  R. Andersen,et al.  Encoding of three-dimensional structure-from-motion by primate area MT neurons , 1998, Nature.

[6]  R. Desimone,et al.  Stimulus-selective properties of inferior temporal neurons in the macaque , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[7]  K Nakayama,et al.  Visual attention to surfaces in three-dimensional space. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[8]  G. V. Van Hoesen,et al.  Prosopagnosia , 1982, Neurology.

[9]  Nancy Kanwisher,et al.  fMRI evidence for objects as the units of attentional selection , 1999, Nature.

[10]  F. Qiu,et al.  Figure and Ground in the Visual Cortex: V2 Combines Stereoscopic Cues with Gestalt Rules , 2005, Neuron.

[11]  M. Valdés-Sosa,et al.  Switching Attention without Shifting the Spotlight: Object-Based Attentional Modulation of Brain Potentials , 1998, Journal of Cognitive Neuroscience.

[12]  Erik Blaser,et al.  Tracking an object through feature space , 2000, Nature.

[13]  Valia Rodríguez,et al.  Sensory suppression during shifts of attention between surfaces in transparent motion , 2006, Brain Research.

[14]  A M Dale,et al.  Optimal experimental design for event‐related fMRI , 1999, Human brain mapping.

[15]  N. Kanwisher,et al.  The Fusiform Face Area: A Module in Human Extrastriate Cortex Specialized for Face Perception , 1997, The Journal of Neuroscience.

[16]  Smith-Kettlewell Neural correlates of object-based attention , 2002 .

[17]  Mazyar Fallah,et al.  Stimulus-specific competitive selection in macaque extrastriate visual area V4 , 2007, Proceedings of the National Academy of Sciences.

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

[19]  Geoffrey M. Boynton,et al.  Efficient Design of Event-Related fMRI Experiments Using M-Sequences , 2002, NeuroImage.

[20]  Valia Rodríguez,et al.  Two-object attentional interference depends on attentional set. , 2004, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[21]  Jens Schwarzbach,et al.  Control of object-based attention in human cortex. , 2004, Cerebral cortex.

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

[23]  E. DeYoe,et al.  A physiological correlate of the 'spotlight' of visual attention , 1999, Nature Neuroscience.

[24]  D. B. Bender,et al.  Visual properties of neurons in inferotemporal cortex of the Macaque. , 1972, Journal of neurophysiology.

[25]  D. Heeger,et al.  Spatial attention affects brain activity in human primary visual cortex. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[26]  Marlene Behrmann,et al.  Cortical systems mediating visual attention to both objects and spatial locations. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

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

[28]  Georgina M. Blanc,et al.  Exploring the mechanisms underlying surface-based stimulus selection , 2010, Vision Research.

[29]  Andreas Kleinschmidt,et al.  Dynamic Interaction of Object- and Space-Based Attention in Retinotopic Visual Areas , 2003, The Journal of Neuroscience.

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

[31]  M. Valdés-Sosa,et al.  Transparent motion and object-based attention , 1998, Cognition.

[32]  Jude F. Mitchell,et al.  Attentional selection of superimposed surfaces cannot be explained by modulation of the gain of color channels , 2003, Vision Research.

[33]  Stefan Treue,et al.  Visual attention: of features and transparent surfaces , 2007, Trends in Cognitive Sciences.

[34]  J. Reynolds,et al.  Exogenous attentional selection of transparent superimposed surfaces modulates early event-related potentials , 2005, Vision Research.

[35]  Vivian M Ciaramitaro,et al.  Spatial and cross-modal attention alter responses to unattended sensory information in early visual and auditory human cortex. , 2007, Journal of neurophysiology.

[36]  Takeo Watanabe,et al.  Separate Processing of Different Global-Motion Structures in Visual Cortex Is Revealed by fMRI , 2005, Current Biology.

[37]  Mitchell Valdes-Sosa,et al.  Attentional shifts between surfaces: effects on detection and early brain potentials , 2001, Vision Research.

[38]  D. Watt Visual Processing: Computational Psychophysical and Cognitive Research , 1990 .

[39]  J. Reynolds,et al.  Attentional modulation of visual processing. , 2004, Annual review of neuroscience.

[40]  Winrich A. Freiwald,et al.  Attention to objects made of features , 2007, Trends in Cognitive Sciences.