Spatially Specific Attention Mechanisms Are Sensitive to Competition during Visual Search

Extensive studies have focused on selection mechanisms during visual search. One important influence on these mechanisms is the perceptual characteristics of the stimuli. We investigated the impact of perceptual similarity between targets and nontargets (T-N similarity) in a visual search task using EEG. Participants searched for a predefined target letter among five nontargets. The T-N similarity was manipulated with three levels: high, middle, and low. We tested for the influences of T-N similarity on an ERP (e.g., N2pc) and alpha oscillations. We observed a significant N2pc effect across all levels of similarity. The N2pc amplitude was reduced and occurred later for high similarity relative to low and middle similarities. We also showed that the N2pc amplitude was inversely correlated with the RTs across all similarities. Importantly, we found a significant alpha phase adjustment about the same time as the N2pc for high similarity; by contrast, no such effect was observed for middle and low similarities. Finally, we showed a positive correlation between the phase-locking value and the N2pc—the stronger the alpha phase-locking value, the larger the N2pc, when the T-N similarity was high. In conclusion, our results provide novel evidence for multiple competitive mechanisms during visual search.

[1]  Christoph M. Michel,et al.  A bias for posterior α-band power suppression versus enhancement during shifting versus maintenance of spatial attention , 2009, NeuroImage.

[2]  Jeff Miller,et al.  Jackknife-based method for measuring LRP onset latency differences. , 1998, Psychophysiology.

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

[4]  Robert Oostenveld,et al.  FieldTrip: Open Source Software for Advanced Analysis of MEG, EEG, and Invasive Electrophysiological Data , 2010, Comput. Intell. Neurosci..

[5]  Agnieszka Wykowska,et al.  Context heterogeneity has a sustained impact on attention deployment: behavioral and electrophysiological evidence. , 2013, Psychophysiology.

[6]  Martin Eimer,et al.  The N2pc component and its links to attention shifts and spatially selective visual processing. , 2008, Psychophysiology.

[7]  Jeffrey R W Mounts,et al.  Competitive interaction degrades target selection: an ERP study. , 2009, Psychophysiology.

[8]  J. Townsend.  Theoretical analysis of an alphabetic confusion matrix , 1971 .

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

[10]  A Treisman,et al.  Feature analysis in early vision: evidence from search asymmetries. , 1988, Psychological review.

[11]  Robert Sekuler,et al.  The Importance of Ignoring , 2014, Current directions in psychological science.

[12]  Kait Clark,et al.  Visual search performance is predicted by both prestimulus and poststimulus electrical brain activity , 2016, Scientific Reports.

[13]  R. Oostenveld,et al.  Nonparametric statistical testing of EEG- and MEG-data , 2007, Journal of Neuroscience Methods.

[14]  S J Luck,et al.  Spatial filtering during visual search: evidence from human electrophysiology. , 1994, Journal of experimental psychology. Human perception and performance.

[15]  J. Pernier,et al.  Stimulus Specificity of Phase-Locked and Non-Phase-Locked 40 Hz Visual Responses in Human , 1996, The Journal of Neuroscience.

[16]  Á. Pascual-Leone,et al.  α-Band Electroencephalographic Activity over Occipital Cortex Indexes Visuospatial Attention Bias and Predicts Visual Target Detection , 2006, The Journal of Neuroscience.

[17]  R. VanRullen,et al.  An oscillatory mechanism for prioritizing salient unattended stimuli , 2012, Trends in Cognitive Sciences.

[18]  M. Eimer,et al.  Electrophysiological markers of visual dimension changes and response changes. , 2008, Journal of experimental psychology. Human perception and performance.

[19]  W. Klimesch.  Alpha-band oscillations, attention, and controlled access to stored information , 2012, Trends in Cognitive Sciences.

[20]  J. Wolfe,et al.  Guided Search 2.0 A revised model of visual search , 1994, Psychonomic bulletin & review.

[21]  P. Roelfsema,et al.  Different States in Visual Working Memory: When It Guides Attention and When It Does Not , 2022 .

[22]  A. Schubö,et al.  Target discrimination delays attentional benefit for grouped contexts: An ERP study , 2015, Brain Research.

[23]  J. Schoffelen,et al.  University of Birmingham Occipital alpha activity during stimulus processing gates the information flow to object-selective cortex , 2014 .

[24]  O. Jensen,et al.  Alpha Oscillations Serve to Protect Working Memory Maintenance against Anticipated Distracters , 2012, Current Biology.

[25]  Jöran Lepsien,et al.  Searching for Targets within the Spatial Layout of Visual Short-Term Memory , 2009, The Journal of Neuroscience.

[26]  Anna Schubö,et al.  You see what you have learned. Evidence for an interrelation of associative learning and visual selective attention. , 2015, Psychophysiology.

[27]  A. Karim,et al.  Brain Oscillatory Substrates of Visual Short-Term Memory Capacity , 2009, Current Biology.

[28]  Leslie G. Ungerleider,et al.  Mechanisms of visual attention in the human cortex. , 2000, Annual review of neuroscience.

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

[30]  Diane M. Beck,et al.  To See or Not to See: Prestimulus α Phase Predicts Visual Awareness , 2009, The Journal of Neuroscience.

[31]  A. Nobre,et al.  Oscillatory Brain State Predicts Variability in Working Memory , 2014, The Journal of Neuroscience.

[32]  Steven J. Luck,et al.  Lateralized Suppression of Alpha-Band EEG Activity As a Mechanism of Target Processing , 2018, The Journal of Neuroscience.

[33]  C. C. Wood,et al.  The ɛ-Adjustment Procedure for Repeated-Measures Analyses of Variance , 1976 .

[34]  James W Bisley,et al.  The what, where, and why of priority maps and their interactions with visual working memory , 2015, Annals of the New York Academy of Sciences.

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

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

[37]  G. V. Simpson,et al.  Anticipatory Biasing of Visuospatial Attention Indexed by Retinotopically Specific α-Bank Electroencephalography Increases over Occipital Cortex , 2000, The Journal of Neuroscience.

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

[39]  Martin Eimer,et al.  Activation of New Attentional Templates for Real-world Objects in Visual Search , 2015, Journal of Cognitive Neuroscience.

[40]  Bradley R. Postle,et al.  Decoding and Reconstructing the Focus of Spatial Attention from the Topography of Alpha-band Oscillations , 2016, Journal of Cognitive Neuroscience.

[41]  R. C. Oldfield.  THE ASSESSMENT AND ANALYSIS OF HANDEDNESS , 1971 .

[42]  Edward K Vogel,et al.  Neural Evidence for the Contribution of Active Suppression During Working Memory Filtering , 2019, Cerebral cortex.

[43]  M. Eimer.  The N2pc component as an indicator of attentional selectivity. , 1996, Electroencephalography and clinical neurophysiology.

[44]  Paige E. Scalf,et al.  Competition in Visual Cortex Impedes Attention to Multiple Items , 2010, The Journal of Neuroscience.

[45]  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.

[46]  Ole Jensen,et al.  Alpha Oscillations Correlate with the Successful Inhibition of Unattended Stimuli , 2011, Journal of Cognitive Neuroscience.

[47]  R. VanRullen,et al.  The Phase of Ongoing Oscillations Mediates the Causal Relation between Brain Excitation and Visual Perception , 2011, The Journal of Neuroscience.

[48]  J. Gross,et al.  Sounds Reset Rhythms of Visual Cortex and Corresponding Human Visual Perception , 2012, Current Biology.

[49]  L. Chelazzi.  Serial attention mechanisms in visual search: A critical look at the evidence , 1999, Psychological research.

[50]  John J. Foxe,et al.  Increases in alpha oscillatory power reflect an active retinotopic mechanism for distracter suppression during sustained visuospatial attention. , 2006, Journal of neurophysiology.

[51]  S. Luck,et al.  Neural sources of focused attention in visual search. , 2000, Cerebral cortex.

[52]  Martin Eimer,et al.  Spatial Attention Can Be Allocated Rapidly and in Parallel to New Visual Objects , 2014, Current Biology.

[53]  S. Luck,et al.  A Common Neural Mechanism for Preventing and Terminating the Allocation of Attention , 2012, The Journal of Neuroscience.

[54]  C. Bundesen.  A theory of visual attention. , 1990, Psychological review.

[55]  Y. Yeh,et al.  Top-down modulation of alpha power and pattern similarity for threatening representations in visual short-term memory , 2017, Neuropsychologia.

[56]  S. Kastner,et al.  From Behavior to Neural Dynamics: An Integrated Theory of Attention , 2015, Neuron.

[57]  Martin Eimer,et al.  Rapid parallel attentional target selection in single-color and multiple-color visual search. , 2015, Journal of experimental psychology. Human perception and performance.

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

[59]  A. Caramazza,et al.  An electrophysiological assessment of distractor suppression in visual search tasks. , 2009, Psychophysiology.

[60]  Steven J. Luck,et al.  Combined Electrophysiological and Behavioral Evidence for the Suppression of Salient Distractors , 2018, Journal of Cognitive Neuroscience.

[61]  Anna Christina Nobre,et al.  Top–Down Activation of Spatiotopic Sensory Codes in Perceptual and Working Memory Search , 2016, Journal of Cognitive Neuroscience.

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

[63]  Diane M. Beck,et al.  Top-down and bottom-up mechanisms in biasing competition in the human brain , 2009, Vision Research.

[64]  Shane T. Mueller,et al.  Alphabetic letter identification: effects of perceivability, similarity, and bias. , 2012, Acta psychologica.

[65]  C. Koch,et al.  Computational modelling of visual attention , 2001, Nature Reviews Neuroscience.

[66]  R. VanRullen,et al.  The phase of ongoing EEG oscillations predicts visual perception , 2010 .

[67]  J. Duncan,et al.  Visual search and stimulus similarity. , 1989, Psychological review.

[68]  R. Romo,et al.  α-Oscillations in the monkey sensorimotor network influence discrimination performance by rhythmical inhibition of neuronal spiking , 2011, Proceedings of the National Academy of Sciences.

[69]  Veronica Mazza,et al.  Attentional processing of multiple targets and distractors. , 2013, Psychophysiology.

[70]  Sammi R. Chekroud,et al.  Concurrent visual and motor selection during visual working memory guided action , 2018, Nature Neuroscience.

[71]  Robert Sekuler,et al.  Attention-modulated Alpha-band Oscillations Protect against Intrusion of Irrelevant Information , 2013, Journal of Cognitive Neuroscience.

[72]  P. Jolicoeur,et al.  Early and late selection processes have separable influences on the neural substrates of attention. , 2018, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[73]  O. Jensen,et al.  Shaping Functional Architecture by Oscillatory Alpha Activity: Gating by Inhibition , 2010, Front. Hum. Neurosci..

[74]  C C Wood,et al.  Letter: The epsilon-adjustment procedure for repeated-measures analyses of variance. , 1976, Psychophysiology.

[75]  A. Treisman,et al.  A feature-integration theory of attention , 1980, Cognitive Psychology.

[76]  R. C. Oldfield.  The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[77]  P. Jolicoeur,et al.  Early and late selection modulate competition for representation: Evidence from the N2pc in a multiple frame procedure. , 2016, Psychophysiology.

[78]  Edward Awh,et al.  Alpha-Band Oscillations Enable Spatially and Temporally Resolved Tracking of Covert Spatial Attention , 2017, Psychological science.

[79]  W. Klimesch,et al.  EEG alpha oscillations: The inhibition–timing hypothesis , 2007, Brain Research Reviews.

[80]  Leslie G. Ungerleider,et al.  The neural basis of biased competition in human visual cortex , 2001, Neuropsychologia.

[81]  M. Eimer.  The neural basis of attentional control in visual search , 2014, Trends in Cognitive Sciences.

[82]  Jöran Lepsien,et al.  Purely endogenous capture of attention by task-defining features proceeds independently from spatial attention , 2010, NeuroImage.