Preparatory Effects of Distractor Suppression: Evidence from Visual Cortex

Spatial selective attention is the mechanism that facilitates the selection of relevant information over irrelevant information in the visual field. The current study investigated whether foreknowledge of the presence or absence of distractors surrounding an impending target stimulus results in preparatory changes in visual cortex. We cued the location of the target and the presence or absence of distractors surrounding the target while changes in blood oxygen level dependent (BOLD) signals were measured. In line with prior work, we found that top-down spatial attention resulted in an increased contralateral BOLD response, evoked by the cue throughout early visual cortex (areas V1, V2 and V3). In addition, cues indicating distractor presence evoked a substantial increase in the magnitude of the BOLD signal in visual area V3, but not in V2 or V1. This study shows that prior knowledge concerning the presence of a distractor results in enhanced attentional modulation of visual cortex, in visual areas where neuronal receptive fields are large enough to encompass both targets and distractors. We interpret these findings as evidence that top-down attentional control processes include active preparatory suppression mechanisms for irrelevant, distracting information in the visual scene.

[1]  M. Posner,et al.  Orienting of Attention* , 1980, The Quarterly journal of experimental psychology.

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

[3]  C. Eriksen,et al.  Visual attention within and around the field of focal attention: A zoom lens model , 1986, Perception & psychophysics.

[4]  D. V. van Essen,et al.  Processing of color, form and disparity information in visual areas VP and V2 of ventral extrastriate cortex in the macaque monkey , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[5]  M. Torrens Co-Planar Stereotaxic Atlas of the Human Brain—3-Dimensional Proportional System: An Approach to Cerebral Imaging, J. Talairach, P. Tournoux. Georg Thieme Verlag, New York (1988), 122 pp., 130 figs. DM 268 , 1990 .

[6]  A. H. C. van der Heijden,et al.  Selective Attention in Vision , 1991 .

[7]  M. Gazzaniga,et al.  Combined spatial and temporal imaging of brain activity during visual selective attention in humans , 1994, Nature.

[8]  H. Pashler,et al.  Negligible Effect of Spatial Precuing on Identification of Single Digits , 1994 .

[9]  R. Desimone,et al.  Neural mechanisms of selective visual attention. , 1995, Annual review of neuroscience.

[10]  S J Luck,et al.  Mechanisms of visual-spatial attention: resource allocation or uncertainty reduction? , 1996, Journal of experimental psychology. Human perception and performance.

[11]  G A Orban,et al.  Attention to One or Two Features in Left or Right Visual Field: A Positron Emission Tomography Study , 1997, The Journal of Neuroscience.

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

[13]  A. Dale,et al.  The Retinotopy of Visual Spatial Attention , 1998, Neuron.

[14]  Leslie G. Ungerleider,et al.  Mechanisms of directed attention in the human extrastriate cortex as revealed by functional MRI. , 1998, Science.

[15]  E. Vogel,et al.  Sensory gain control (amplification) as a mechanism of selective attention: electrophysiological and neuroimaging evidence. , 1998, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

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

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

[18]  Leslie G. Ungerleider,et al.  Increased Activity in Human Visual Cortex during Directed Attention in the Absence of Visual Stimulation , 1999, Neuron.

[19]  Eileen Kowler,et al.  Attentional interference at small spatial separations , 1999, Vision Research.

[20]  A. Borst Seeing smells: imaging olfactory learning in bees , 1999, Nature Neuroscience.

[21]  D. Somers,et al.  Functional MRI reveals spatially specific attentional modulation in human primary visual cortex. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[22]  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.

[23]  H. Pashler,et al.  Evidence for split attentional foci. , 2000, Journal of experimental psychology. Human perception and performance.

[24]  J. R. Mounts,et al.  Attentional capture by abrupt onsets and feature singletons produces inhibitory surrounds , 2000, Perception & psychophysics.

[25]  M. Carrasco,et al.  Spatial covert attention increases contrast sensitivity across the CSF: support for signal enhancement , 2000, Vision Research.

[26]  D. Heeger,et al.  Activity in primary visual cortex predicts performance in a visual detection task , 2000, Nature Neuroscience.

[27]  J. R. Mounts Evidence for suppressive mechanisms in attentional selection: Feature singletons produce inhibitory surrounds , 2000, Perception & psychophysics.

[28]  G. Mangun,et al.  The neural mechanisms of top-down attentional control , 2000, Nature Neuroscience.

[29]  A. T. Smith,et al.  Estimating receptive field size from fMRI data in human striate and extrastriate visual cortex. , 2001, Cerebral cortex.

[30]  M. Corbetta,et al.  Separating Processes within a Trial in Event-Related Functional MRI II. Analysis , 2001, NeuroImage.

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

[32]  Steven Yantis,et al.  Efficient acquisition of human retinotopic maps , 2003, Human brain mapping.

[33]  J. Serences,et al.  Top-down control over biased competition during covert spatial orienting. , 2003, Journal of experimental psychology. Human perception and performance.

[34]  A. Dale,et al.  Functional Parcellation of Attentional Control Regions of the Brain , 2004, Journal of Cognitive Neuroscience.

[35]  Notger G. Müller,et al.  The attentional ‘spotlight's’ penumbra: center-surround modulation in striate cortex , 2004, Neuroreport.

[36]  S. Yantis,et al.  Preparatory activity in visual cortex indexes distractor suppression during covert spatial orienting. , 2004, Journal of neurophysiology.

[37]  A. Kleinschmidt,et al.  The attentional field has a Mexican hat distribution , 2005, Vision Research.

[38]  Hans-Jochen Heinze,et al.  The Neural Site of Attention Matches the Spatial Scale of Perception , 2006, The Journal of Neuroscience.

[39]  John K. Tsotsos,et al.  Direct neurophysiological evidence for spatial suppression surrounding the focus of attention in vision. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[40]  M. Corbetta,et al.  Separate Modulations of Human V1 Associated with Spatial Attention and Task Structure , 2006, Neuron.

[41]  Jon Driver,et al.  Attentional Preparation for a Lateralized Visual Distractor: Behavioral and fMRI Evidence , 2006, Journal of Cognitive Neuroscience.

[42]  David J Heeger,et al.  Neural correlates of sustained spatial attention in human early visual cortex. , 2007, Journal of neurophysiology.

[43]  J. Theeuwes,et al.  Directing attention to a location in space results in retinotopic activation in primary visual cortex , 2008, Brain Research.

[44]  J. Theeuwes,et al.  Cueing the location of a distractor: an inhibitory mechanism of spatial attention? , 2008, Acta psychologica.

[45]  G. Mangun,et al.  Signal enhancement and suppression during visual–spatial selective attention , 2010, Brain Research.