Enhanced spatial focusing increases feature-based selection in unattended locations

Attention is a multifaceted phenomenon, which operates on features (e.g., colour or motion) and over space. A fundamental question is whether the attentional selection of features is confined to the spatially-attended location or operates independently across the entire visual field (global feature-based attention, GFBA). Studies providing evidence for GFBA often employ feature probes presented at spatially unattended locations, which elicit enhanced brain responses when they match a currently-attended target feature. However, the validity of this interpretation relies on consistent spatial focusing onto the target. If the probe were to temporarily attract spatial attention, the reported effects could reflect transient spatial selection processes, rather than GFBA. Here, using magnetoencephalographic recordings (MEG) in humans, we manipulate the strength and consistency of spatial focusing to the target by increasing the target discrimination difficulty (Experiment 1), and by demarcating the upcoming target’s location with a placeholder (Experiment 2), to see if GFBA effects are preserved. We observe that motivating stronger spatial focusing to the target did not diminish the effects of GFBA. Instead, aiding spatial pre-focusing with a placeholder enhanced the feature response at unattended locations. Our findings confirm that feature selection effects measured with spatially-unattended probes reflect a true location-independent neural bias.

[1]  J. Gallant,et al.  Time Course of Attention Reveals Different Mechanisms for Spatial and Feature-Based Attention in Area V4 , 2005, Neuron.

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

[3]  C. Folk,et al.  Target-uncertainty effects in attentional capture: Color-singleton set or multiple attentional control settings? , 2010, Psychonomic bulletin & review.

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

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

[6]  D. LaBerge,et al.  Reducing the effects of adjacent distractors by narrowing attention. , 1991, Journal of experimental psychology. Human perception and performance.

[7]  B. Motter Neural correlates of attentive selection for color or luminance in extrastriate area V4 , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[8]  H J Müller,et al.  Movement versus focusing of visual attention , 1989, Perception & psychophysics.

[9]  Marina Schmid,et al.  An Introduction To The Event Related Potential Technique , 2016 .

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

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

[12]  S. Yantis,et al.  Abrupt visual onsets and selective attention: voluntary versus automatic allocation. , 1990, Journal of experimental psychology. Human perception and performance.

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

[14]  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.

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

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

[17]  John M. Gaspar,et al.  Suppression of Salient Objects Prevents Distraction in Visual Search , 2014, The Journal of Neuroscience.

[18]  G. Sperling,et al.  Is there feature-based attentional selection in visual search? , 1996, Journal of experimental psychology. Human perception and performance.

[19]  Clayton Hickey,et al.  Target resolution in visual search involves the direct suppression of distractors: evidence from electrophysiology. , 2012, Psychophysiology.

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

[21]  Anna C. Nobre,et al.  Synergistic Effect of Combined Temporal and Spatial Expectations on Visual Attention , 2005, The Journal of Neuroscience.

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

[23]  Hans-Jochen Heinze,et al.  Localizing visual discrimination processes in time and space. , 2002, Journal of neurophysiology.

[24]  Hans-Jochen Heinze,et al.  Determinants of Global Color-Based Selection in Human Visual Cortex. , 2015, Cerebral cortex.

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

[26]  S A Hillyard,et al.  Feature-selective attention enhances color signals in early visual areas of the human brain , 2006, Proceedings of the National Academy of Sciences.

[27]  Gijsbertus Mulder,et al.  An electrophysiological investigation of the spatial distribution of attention to colored stimuli in focused and divided attention conditions , 1989, Biological Psychology.

[28]  A C Nobre,et al.  Preparatory α-band oscillations reflect spatial gating independently of predictions regarding target identity. , 2017, Journal of neurophysiology.

[29]  S. Hillyard,et al.  Selective attention to the color and direction of moving stimuli: Electrophysiological correlates of hierarchical feature selection , 1996, Perception & psychophysics.

[30]  S. Yantis,et al.  Visual attention: control, representation, and time course. , 1997, Annual review of psychology.

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

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

[33]  Hans-Jochen Heinze,et al.  Cortical Mechanisms of Prioritizing Selection for Rejection in Visual Search , 2018, The Journal of Neuroscience.

[34]  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.

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

[36]  Verena C. Seibold,et al.  Toward the influence of temporal attention on the selection of targets in a visual search task: An ERP study. , 2016, Psychophysiology.

[37]  Jason T. Arita,et al.  A cuing study of the N2pc component: An index of attentional deployment to objects rather than spatial locations , 2009, Brain Research.

[38]  N. Lavie,et al.  On the Efficiency of Visual Selective Attention: Efficient Visual Search Leads to Inefficient Distractor Rejection , 1997 .

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

[40]  J. C. Johnston,et al.  Involuntary covert orienting is contingent on attentional control settings. , 1992, Journal of experimental psychology. Human perception and performance.

[41]  Carly J. Leonard,et al.  Interactions between space-based and feature-based attention. , 2015, Journal of experimental psychology. Human perception and performance.

[42]  J. Theeuwes Exogenous and endogenous control of attention: The effect of visual onsets and offsets , 1991, Perception & psychophysics.

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

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

[45]  A. Mizuno,et al.  A change of the leading player in flow Visualization technique , 2006, J. Vis..

[46]  D. Heeger,et al.  The Normalization Model of Attention , 2009, Neuron.

[47]  M. Eimer Event-related potential correlates of transient attention shifts to color and location , 1995, Biological Psychology.

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

[49]  S. Hillyard,et al.  Modulations of sensory-evoked brain potentials indicate changes in perceptual processing during visual-spatial priming. , 1991, Journal of experimental psychology. Human perception and performance.

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

[51]  S. Hillyard,et al.  Selective attention to color and location: An analysis with event-related brain potentials , 1984, Perception & psychophysics.

[52]  H. Egeth,et al.  Are attentional dwell times inconsistent with serial visual search? , 1996, Psychonomic bulletin & review.

[53]  Lisa N. Jefferies,et al.  When can spatial attention be deployed in the form of an annulus? , 2014, Attention, Perception, & Psychophysics.

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

[55]  Steven A. Hillyard,et al.  Attention Facilitates Multiple Stimulus Features in Parallel in Human Visual Cortex , 2008, Current Biology.

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

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

[58]  K. Nakayama,et al.  Sustained and transient components of focal visual attention , 1989, Vision Research.

[59]  H. Spitzer,et al.  Increased attention enhances both behavioral and neuronal performance. , 1988, Science.

[60]  Y. Tsal,et al.  Location dominance in attending to color and shape. , 1993, Journal of experimental psychology. Human perception and performance.

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

[62]  J. Theeuwes,et al.  Abrupt onsets capture attention independent of top-down control settings , 2008, Perception & psychophysics.

[63]  B. Gibson,et al.  Stimulus-driven attentional capture is contingent on attentional set for displaywide visual features. , 1998, Journal of experimental psychology. Human perception and performance.

[64]  H. Spitzer,et al.  Task difficulty: ignoring, attending to, and discriminating a visual stimulus yield progressively more activity in inferior temporal neurons , 2004, Experimental Brain Research.

[65]  G. Mangun,et al.  Perceptual Load and Visuocortical Processing: Event-Related Potentials Reveal Sensory-Level Selection , 2001, Psychological science.

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

[67]  Steven J. Luck,et al.  The Role of Inhibition in Avoiding Distraction by Salient Stimuli , 2018, Trends in Cognitive Sciences.

[68]  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.

[69]  Hans-Jochen Heinze,et al.  Attention to Color Sharpens Neural Population Tuning via Feedback Processing in the Human Visual Cortex Hierarchy , 2017, The Journal of Neuroscience.

[70]  M Corbetta,et al.  Attentional modulation of neural processing of shape, color, and velocity in humans. , 1990, Science.

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

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

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