Attention-modulated activity in visual cortex—More than a simple ‘spotlight’

We assessed modulation of retinotopic visual cortex representing peripheral regions of the visual field while subjects engaged in a central attention task. The onset of an attention capturing central letter stream attenuated activity in representations of the peripheral locations. When these locations were empty, the observed reduction was the same whether subjects passively viewed or actively attended the letter stream. For locations containing distracting letters, however, an additional attenuation was observed during the active task. In a second experiment we found that representations of target incompatible peripheral letters were suppressed relative to a control task, whereas at the same time representations of compatible peripheral letters were relatively enhanced. The fMRI results are complemented by behavioral data demonstrating prolonged responses to probes presented at suppressed locations. In sum, our study suggests that activity modulation across the visual field representation not only reflects an attentional spotlight effect but is additionally shaped by the nature of sensory input at unattended locations as well as its relation to task demands.

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

[2]  N. Lavie Perceptual load as a necessary condition for selective attention. , 1995, Journal of experimental psychology. Human perception and performance.

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

[4]  C D Frith,et al.  Modulating irrelevant motion perception by varying attentional load in an unrelated task. , 1997, Science.

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

[6]  M. Molteni,et al.  Is attentional focusing an inhibitory process at distractor location? , 2000, Brain research. Cognitive brain research.

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

[8]  Arno Villringer,et al.  A Physiological Correlate of the “Zoom Lens” of Visual Attention , 2003, The Journal of Neuroscience.

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

[10]  C. Eriksen,et al.  How much processing do nonattended stimuli receive? Apparently very little, but... , 1990, Perception & psychophysics.

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

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

[13]  Raymond Klein,et al.  Inhibitory tagging system facilitates visual search , 1988, Nature.

[14]  A. T. Smith,et al.  Attentional suppression of activity in the human visual cortex , 2000, Neuroreport.

[15]  M. Pinsk,et al.  Push-pull mechanism of selective attention in human extrastriate cortex. , 2004, Journal of neurophysiology.

[16]  B. Fischer,et al.  Visual field representations and locations of visual areas V1/2/3 in human visual cortex. , 2003, Journal of vision.

[17]  I. THE ATTENTION SYSTEM OF THE HUMAN BRAIN , 2002 .

[18]  N. P. Bichot,et al.  Spatial selection via feature-driven inhibition of distractor locations , 1998, Perception & psychophysics.

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

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

[21]  C. Eriksen,et al.  Selective attention: Noise suppression or signal enhancement? , 1974 .

[22]  R. Knight,et al.  Prefrontal modulation of visual processing in humans , 2000, Nature Neuroscience.

[23]  Scott D Slotnick,et al.  Darkness beyond the light: attentional inhibition surrounding the classic spotlight , 2002, Neuroreport.

[24]  Andreas Kleinschmidt,et al.  Temporal Dynamics of the Attentional Spotlight: Neuronal Correlates of Attentional Capture and Inhibition of Return in Early Visual Cortex , 2007, Journal of Cognitive Neuroscience.

[25]  Scott B. Steinman,et al.  Visual attention mechanisms show a center—surround organization , 1995, Vision Research.

[26]  M Corbetta,et al.  Frontoparietal cortical networks for directing attention and the eye to visual locations: identical, independent, or overlapping neural systems? , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[27]  John K. Tsotsos,et al.  The selective tuning model of attention: psychophysical evidence for a suppressive annulus around an attended item , 2003, Vision Research.

[28]  J H Flowers,et al.  The effect of flanking context on visual classification: The joint contribution of interactions at different processing levels , 1982, Perception & psychophysics.

[29]  G. Caputo,et al.  Attentional selection by distractor suppression , 1998, Vision Research.

[30]  M. Carrasco,et al.  Transient Attention Enhances Perceptual Performance and fMRI Response in Human Visual Cortex , 2005, Neuron.

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

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

[33]  M I Sereno,et al.  Analysis of retinotopic maps in extrastriate cortex. , 1994, Cerebral cortex.

[34]  M. Corbetta,et al.  Control of goal-directed and stimulus-driven attention in the brain , 2002, Nature Reviews Neuroscience.

[36]  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.

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

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

[39]  M. Posner,et al.  Attention and the detection of signals. , 1980, Journal of experimental psychology.

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

[41]  Y. Tsal,et al.  Perceptual load as a major determinant of the locus of selection in visual attention , 1994, Perception & psychophysics.

[42]  D. Somers,et al.  Multiple Spotlights of Attentional Selection in Human Visual Cortex , 2004, Neuron.

[43]  Charles Curtis Eriksen,et al.  The extent of processing of noise elements during selective encoding from visual displays , 1973 .

[44]  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.

[45]  R. Dolan,et al.  Attentional load and sensory competition in human vision: modulation of fMRI responses by load at fixation during task-irrelevant stimulation in the peripheral visual field. , 2005, Cerebral cortex.

[46]  A. Facoetti Facilitation and inhibition mechanisms of human visuospatial attention in a non-search task , 2001, Neuroscience Letters.

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