Temporal Dynamics of the Attentional Spotlight: Neuronal Correlates of Attentional Capture and Inhibition of Return in Early Visual Cortex

A stimulus that suddenly appears in the corner of the eye inevitably captures our attention, and this in turn leads to faster detection of a second stimulus presented at the same position shortly thereafter. After about 250 msec, however, this effect reverses and the second stimulus is detected faster when it appears far away from the first. Here, we report a potential physiological correlate of this time-dependent attentional facilitation and inhibition. We measured the activity in visual cortex representations of the second (target) stimulus' location depending on the stimulus onset asynchrony (SOA) and spatial distance that separated the target from the preceding cue stimulus. At an SOA of 100 msec, the target yielded larger responses when it was presented near to than far away from the cue. At an SOA of 850 msec, however, the response to the target was more pronounced when it appeared far away from the cue. Our data show how the neural substrate of visual orienting is guided by immediately preceding sensory experience and how a fast-reacting brain system modulates sensory processing by briefly increasing and subsequently decreasing responsiveness in parts of the visual cortex. We propose these activity modulations as the neural correlate of the sequence of perceptual facilitation and inhibition after attentional capture.

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

[2]  Notger G. Müller,et al.  Attention-modulated activity in visual cortex—More than a simple ‘spotlight’ , 2008, NeuroImage.

[3]  L. Anllo-Vento Shifting attention in visual space: the effects of peripheral cueing on brain cortical potentials. , 1995, The International journal of neuroscience.

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

[5]  M. Posner,et al.  Components of visual orienting , 1984 .

[6]  R. Klein,et al.  Inhibition of return , 2000, Trends in Cognitive Sciences.

[7]  M. Eimer An ERP study on visual spatial priming with peripheral onsets. , 1994, Psychophysiology.

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

[9]  E. Maylor,et al.  Inhibitory component of externally controlled covert orienting in visual space. , 1985, Journal of experimental psychology. Human perception and performance.

[10]  M. Posner,et al.  Inhibition of return : Neural basis and function , 1985 .

[11]  R. Klein,et al.  Contribution of the Primate Superior Colliculus to Inhibition of Return , 2002, Journal of Cognitive Neuroscience.

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

[13]  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 .

[14]  Notger G. Müller,et al.  The functional neuroanatomy of visual conjunction search: a parametric fMRI study , 2003, NeuroImage.

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

[16]  Tony Ro,et al.  Inhibition of return and the human frontal eye fields , 2003, Experimental Brain Research.

[17]  S. Pollmann,et al.  Covert Reorienting and Inhibition of Return: An Event-Related fMRI Study , 2002, Journal of Cognitive Neuroscience.

[18]  Pierre Jolicoeur,et al.  Response-selection Conflict Contributes to Inhibition of Return , 2009, Journal of Cognitive Neuroscience.

[19]  Xiaolin Zhou,et al.  Neural correlates of spatial and non-spatial inhibition of return (IOR) in attentional orienting , 2008, Neuropsychologia.

[20]  J. Pratt,et al.  The Spatial Distribution of Inhibition of Return , 2001, Psychological science.

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

[23]  L. M. Ward,et al.  Inhibition of Return From Stimulus to Response , 2004, Psychological science.

[24]  George R. Mangun,et al.  Reflexive Attention Modulates Processing of Visual Stimuli in Human Extrastriate Cortex , 1998, Psychological science.

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

[26]  S. Vanni,et al.  Topography of attention in the primary visual cortex , 2009, The European journal of neuroscience.

[27]  M. Corbetta,et al.  A Common Network of Functional Areas for Attention and Eye Movements , 1998, Neuron.

[28]  K. Heekeren,et al.  Pharmacological modulation of the neural basis underlying inhibition of return (IOR) in the human 5-HT2A agonist and NMDA antagonist model of psychosis , 2008, Psychopharmacology.

[29]  Avishai Henik,et al.  Inhibition of return in spatial attention: direct evidence for collicular generation , 1999, Nature Neuroscience.

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

[31]  Lawrence M. Ward,et al.  An event-related brain potential study of inhibition of return , 1999, Perception & psychophysics.

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

[33]  N. Kanwisher,et al.  The Generality of Parietal Involvement in Visual Attention , 1999, Neuron.

[34]  Andreas Kleinschmidt,et al.  The Attentional Blink Modulates Activity in the Early Visual Cortex , 2009, Journal of Cognitive Neuroscience.

[35]  R Fendrich,et al.  Inhibitory tagging of locations in the blind field of hemianopic patients. , 1997, Consciousness and cognition.

[36]  Steven A. Hillyard,et al.  The Cuing of Attention to Visual Field Locations: Analysis with ERP Recordings , 1994 .