Effects of Visual Scene Complexity on Neural Signatures of Spatial Attention

Spatial selective attention greatly affects our processing of complex visual scenes, yet the way in which the brain selects relevant objects while suppressing irrelevant objects is still unclear. Evidence of these processes has been found using non-invasive electroencephalography (EEG). However, few studies have characterized these measures during attention to dynamic stimuli, and little is known regarding how these measures change with increased scene complexity. Here, we compared attentional modulation of the EEG N1 and alpha power (oscillations between 8–14 Hz) across three visual selective attention tasks. The tasks differed in the number of irrelevant stimuli presented, but all required sustained attention to the orientation trajectory of a lateralized stimulus. In scenes with few irrelevant stimuli, top-down control of spatial attention is associated with strong modulation of both the N1 and alpha power across parietal-occipital channels. In scenes with many irrelevant stimuli in both hemifields, however, top-down control is no longer represented by strong modulation of alpha power, and N1 amplitudes are overall weaker. These results suggest that as a scene becomes more complex, requiring suppression in both hemifields, the neural signatures of top-down control degrade, likely reflecting some limitation in EEG to represent this suppression.

[1]  D. Spalding The Principles of Psychology , 1873, Nature.

[2]  Antoine J. Shahin,et al.  Attentional Gain Control of Ongoing Cortical Speech Representations in a “Cocktail Party” , 2010, The Journal of Neuroscience.

[3]  Matthew D. Hilchey,et al.  Feature integration in basic detection and localization tasks: Insights from the attentional orienting literature , 2018, Attention, Perception, & Psychophysics.

[4]  D H Brainard,et al.  The Psychophysics Toolbox. , 1997, Spatial vision.

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

[6]  Søren K. Andersen,et al.  Sustained Multifocal Attentional Enhancement of Stimulus Processing in Early Visual Areas Predicts Tracking Performance , 2013, The Journal of Neuroscience.

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

[8]  John J. Foxe,et al.  The Role of Alpha-Band Brain Oscillations as a Sensory Suppression Mechanism during Selective Attention , 2011, Front. Psychology.

[9]  Denis G. Pelli,et al.  ECVP '07 Abstracts , 2007, Perception.

[10]  S. Dalal,et al.  Prestimulus Oscillatory Phase at 7 Hz Gates Cortical Information Flow and Visual Perception , 2013, Current Biology.

[11]  J. Wolfe,et al.  What is a preattentive feature? , 2019, Current opinion in psychology.

[12]  Jürgen Kayser,et al.  On the benefits of using surface Laplacian (current source density) methodology in electrophysiology. , 2015, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[13]  Arnaud Delorme,et al.  EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis , 2004, Journal of Neuroscience Methods.

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

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

[16]  B. Shinn-Cunningham Object-based auditory and visual attention , 2008, Trends in Cognitive Sciences.

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

[18]  Gregor Thut,et al.  Stimulus-Driven Brain Rhythms within the Alpha Band: The Attentional-Modulation Conundrum , 2018, The Journal of Neuroscience.

[19]  J. Wolfe,et al.  The Invisible Gorilla Strikes Again , 2013, Psychological science.

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

[21]  T. Picton,et al.  The N1 wave of the human electric and magnetic response to sound: a review and an analysis of the component structure. , 1987, Psychophysiology.

[22]  Ted J. Kaptchuk,et al.  Effects of mindfulness meditation training on anticipatory alpha modulation in primary somatosensory cortex , 2011, Brain Research Bulletin.

[23]  Chantal E. Stern,et al.  Long-term memory guidance of visuospatial attention in a change-detection paradigm , 2014, Front. Psychol..

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

[25]  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.

[26]  Robert Sekuler,et al.  Interactions between working memory and visual perception: An ERP/EEG study , 2007, NeuroImage.

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

[28]  T. Horowitz,et al.  Attentional enhancement during multiple-object tracking , 2009, Psychonomic bulletin & review.

[29]  A. Nobre,et al.  Temporal Expectations Guide Dynamic Prioritization in Visual Working Memory through Attenuated α Oscillations , 2017, The Journal of Neuroscience.

[30]  Ronald A. Rensink,et al.  Change blindness: past, present, and future , 2005, Trends in Cognitive Sciences.

[31]  Barbara Shinn-Cunningham,et al.  Individual differences in attentional modulation of cortical responses correlate with selective attention performance , 2014, Hearing Research.

[32]  Michael H. Herzog,et al.  Neural correlates of visual crowding , 2014, NeuroImage.

[33]  Dennis J McFarland,et al.  The advantages of the surface Laplacian in brain-computer interface research. , 2015, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[34]  Manuel Schabus,et al.  A shift of visual spatial attention is selectively associated with human EEG alpha activity , 2005, The European journal of neuroscience.

[35]  Jürgen Kayser,et al.  Principal components analysis of Laplacian waveforms as a generic method for identifying ERP generator patterns: I. Evaluation with auditory oddball tasks , 2006, Clinical Neurophysiology.

[36]  G Pfurtscheller,et al.  Discrimination between phase-locked and non-phase-locked event-related EEG activity. , 1995, Electroencephalography and clinical neurophysiology.

[37]  Lenny A. Varghese,et al.  Quantifying attentional modulation of auditory-evoked cortical responses from single-trial electroencephalography , 2013, Front. Hum. Neurosci..

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

[39]  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.

[40]  K. Nakayama,et al.  Hidden cognitive states revealed in choice reaching tasks , 2009, Trends in Cognitive Sciences.

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

[42]  Virginia Best,et al.  Sensorineural hearing loss degrades behavioral and physiological measures of human spatial selective auditory attention , 2018, Proceedings of the National Academy of Sciences.

[43]  Sven Hoffmann,et al.  The Correction of Eye Blink Artefacts in the EEG: A Comparison of Two Prominent Methods , 2008, PloS one.

[44]  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.

[45]  Lee M. Miller,et al.  The Role of Alpha Activity in Spatial and Feature-Based Attention , 2016, eNeuro.

[46]  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.

[47]  Glyn W. Humphreys,et al.  Feature Confirmation in Object Perception: Feature Integration Theory 26 Years on from the Treisman Bartlett Lecture , 2016, Quarterly journal of experimental psychology.

[48]  C. Chabris,et al.  Gorillas in Our Midst: Sustained Inattentional Blindness for Dynamic Events , 1999, Perception.

[49]  S. Hillyard,et al.  Event-related brain potentials in the study of visual selective attention. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[50]  M. Thulasidas,et al.  Robust classification of EEG signal for brain-computer interface , 2006, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[51]  O. Andreassen,et al.  Mice Deficient in Cellular Glutathione Peroxidase Show Increased Vulnerability to Malonate, 3-Nitropropionic Acid, and 1-Methyl-4-Phenyl-1,2,5,6-Tetrahydropyridine , 2000, The Journal of Neuroscience.

[52]  John J. Foxe,et al.  Oscillatory Alpha-Band Mechanisms and the Deployment of Spatial Attention to Anticipated Auditory and Visual Target Locations: Supramodal or Sensory-Specific Control Mechanisms? , 2011, The Journal of Neuroscience.