Neurophysiological Signals of Ignoring and Attending Are Separable and Related to Performance during Sustained Intersensory Attention

The ability to attend to an input selectively while ignoring distracting sensations is thought to depend on the coordination of two processes: enhancement of target signals and attenuation of distractor signals. This implies that attending and ignoring may be dissociable neural processes and that they make separable contributions to behavioral outcomes of attention. In this study, we tested these hypotheses in the context of sustained attention by measuring neurophysiological responses to attended and ignored stimuli in a noncued, continuous, audiovisual selective attention task. We compared these against responses during a passive control to quantify effects of attending and ignoring separately. In both sensory modalities, responses to ignored stimuli were attenuated relative to a passive control, whereas responses to attended stimuli were enhanced. The scalp topographies and brain activations of these modulatory effects were consistent with the sensory regions that process each modality. They also included parietal and prefrontal activations that suggest these effects arise from interactions between top–down and sensory cortices. Most importantly, we found that both attending and ignoring processes contributed to task accuracy and that these effects were not correlated—suggesting unique neural trajectories. This conclusion was supported by the novel observation that attending and ignoring differed in timing and in active cortical regions. The data provide direct evidence for the separable contributions of attending and ignoring to behavioral outcomes of attention control during sustained intersensory attention.

[1]  Steven A. Hillyard,et al.  Neural Basis of Superior Performance of Action Videogame Players in an Attention-Demanding Task , 2011, The Journal of Neuroscience.

[2]  Gregory V. Simpson,et al.  Biasing the brain’s attentional set: II. Effects of selective intersensory attentional deployments on subsequent sensory processing , 2005, Experimental Brain Research.

[3]  Steven A. Hillyard,et al.  Effects of spatial cuing on luminance detectability: Psychophysical and electrophysiological evidence for early selection. , 1994 .

[4]  S. Hillyard,et al.  Spatial attention to central and peripheral auditory stimuli as indexed by event-related potentials. , 1999, Brain research. Cognitive brain research.

[5]  R. Knight,et al.  Age-related top-down suppression deficit in the early stages of cortical visual memory processing , 2008, Proceedings of the National Academy of Sciences.

[6]  M. D’Esposito,et al.  The effect of non-visual working memory load on top-down modulation of visual processing , 2009, Neuropsychologia.

[7]  Durk Talsma,et al.  Intermodal spatial attention differs between vision and audition: An event-related potential analysis , 2002 .

[8]  Marty G. Woldorff,et al.  Momentary reductions of attention permit greater processing of irrelevant stimuli , 2009, NeuroImage.

[9]  Olivier D. Faugeras,et al.  A common formalism for the Integral formulations of the forward EEG problem , 2005, IEEE Transactions on Medical Imaging.

[10]  Terrence J. Sejnowski,et al.  Independent Component Analysis Using an Extended Infomax Algorithm for Mixed Subgaussian and Supergaussian Sources , 1999, Neural Computation.

[11]  Jon Driver,et al.  Shifts of attention in light and in darkness: an ERP study of supramodal attentional control and crossmodal links in spatial attention. , 2003, Brain research. Cognitive brain research.

[12]  Adam Gazzaley,et al.  Differential coupling of visual cortex with default network or frontal-parietal network based on goals , 2011, Nature Neuroscience.

[13]  G. Mangun Neural mechanisms of visual selective attention. , 1995, Psychophysiology.

[14]  Agatha Lenartowicz,et al.  Updating of context in working memory: An event-related potential study , 2010, Cognitive, affective & behavioral neuroscience.

[15]  R. Näätänen Processing negativity: an evoked-potential reflection of selective attention. , 1982, Psychological bulletin.

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

[17]  Sheila G. Crewther,et al.  Developmental trends in the facilitation of multisensory objects with distractors , 2015, Front. Psychol..

[18]  Phillip J. Holcomb,et al.  Does modulation of selective attention to features reflect enhancement or suppression of neural activity? , 2012, Biological Psychology.

[19]  Lawrence M. Ward,et al.  Electrical Neuroimaging of Voluntary Audiospatial Attention: Evidence for a Supramodal Attention Control Network , 2011, The Journal of Neuroscience.

[20]  Jeffrey W. Cooney,et al.  Top-down suppression deficit underlies working memory impairment in normal aging , 2005, Nature Neuroscience.

[21]  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.

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

[23]  K. Alho,et al.  Intermodal selective attention. I. Effects on event-related potentials to lateralized auditory and visual stimuli. , 1992, Electroencephalography and clinical neurophysiology.

[24]  Richard M. Leahy,et al.  Brainstorm: A User-Friendly Application for MEG/EEG Analysis , 2011, Comput. Intell. Neurosci..

[25]  Jason J S Barton,et al.  Attending to Faces: Change Detection, Familiarization, and Inversion Effects , 2003, Perception.

[26]  Théodore Papadopoulo,et al.  OpenMEEG: opensource software for quasistatic bioelectromagnetics , 2010, Biomedical engineering online.

[27]  R. Gregory The Most Expensive Painting in the World , 2007, Perception.

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

[29]  A. Gazzaley Influence of early attentional modulation on working memory , 2011, Neuropsychologia.

[30]  Steven A. Hillyard,et al.  Effects of Spatial Congruity on Audio-Visual Multimodal Integration , 2005, Journal of Cognitive Neuroscience.

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

[32]  Richard M. Leahy,et al.  Electromagnetic brain mapping , 2001, IEEE Signal Process. Mag..

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

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

[35]  R. Näätänen,et al.  Intermodal selective attention. II. Effects of attentional load on processing of auditory and visual stimuli in central space. , 1992, Electroencephalography and clinical neurophysiology.

[36]  Robert T. Knight,et al.  Top-down Enhancement and Suppression of the Magnitude and Speed of Neural Activity , 2005, Journal of Cognitive Neuroscience.

[37]  Harriet A. Allen,et al.  Active ignoring in early visual cortex , 2010 .

[38]  Robert J. Zatorre,et al.  Neural substrates for dividing and focusing attention between simultaneous auditory and visual events , 2006, NeuroImage.

[39]  Anders M. Dale,et al.  Cortical Surface-Based Analysis I. Segmentation and Surface Reconstruction , 1999, NeuroImage.

[40]  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.

[41]  Nilli Lavie,et al.  Auditory attentional capture: effects of singleton distractor sounds. , 2004, Journal of experimental psychology. Human perception and performance.

[42]  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.

[43]  K. Alho,et al.  Intermodal selective attention: evidence for processing in tonotopic auditory fields. , 1993, Psychophysiology.

[44]  Durk Talsma,et al.  Nonspatial intermodal selective attention is mediated by sensory brain areas: Evidence from event-related potentials , 2001 .

[45]  A. Kok,et al.  Effects of inter- and intramodal selective attention to non-spatial visual stimuli: an event-related potential analysis , 1998, Biological Psychology.

[46]  Jessica J. Green,et al.  An event-related potential study of supramodal attentional control and crossmodal attention effects. , 2006, Psychophysiology.

[47]  S A Hillyard,et al.  Temporal dynamics of human auditory selective attention. , 1988, Psychophysiology.

[48]  E. Saltzman,et al.  Modes of Perceiving and Processing Information , 2014 .

[49]  Maurizio Corbetta,et al.  Anticipatory Suppression of Nonattended Locations in Visual Cortex Marks Target Location and Predicts Perception , 2008, The Journal of Neuroscience.

[50]  Adam Gazzaley,et al.  Early Top–Down Control of Visual Processing Predicts Working Memory Performance , 2010, Journal of Cognitive Neuroscience.

[51]  Adam Gazzaley,et al.  Practice-related improvement in working memory is modulated by changes in processing external interference. , 2009, Journal of neurophysiology.

[52]  T. Uhde,et al.  Differential odor sensitivity in PTSD: Implications for treatment and future research. , 2015, Journal of affective disorders.

[53]  Joseph Biederman,et al.  Attention-deficit/hyperactivity disorder (adhd) as a noradrenergic disorder , 1999, Biological Psychiatry.

[54]  J. Driver,et al.  Crossmodal links in endogenous and exogenous spatial attention: evidence from event-related brain potential studies , 2001, Neuroscience & Biobehavioral Reviews.

[55]  Jessica J. Green,et al.  Electrical Neuroimaging Reveals Timing of Attentional Control Activity in Human Brain , 2008, PLoS Biology.

[56]  S. Hillyard Electrophysiology of human selective attention , 1985, Trends in Neurosciences.

[57]  M. García-Pérez,et al.  Forced-choice staircases with fixed step sizes: asymptotic and small-sample properties , 1998, Vision Research.

[58]  Jeremy R. Reynolds,et al.  Neural Mechanisms of Transient and Sustained Cognitive Control during Task Switching , 2003, Neuron.

[59]  Jonathan D. Cohen,et al.  Role of prefrontal cortex and the midbrain dopamine system in working memory updating , 2012, Proceedings of the National Academy of Sciences.

[60]  A. Dale,et al.  Cortical Surface-Based Analysis II: Inflation, Flattening, and a Surface-Based Coordinate System , 1999, NeuroImage.

[61]  S. Hillyard,et al.  Endogenous brain potentials associated with selective auditory attention. , 1980, Electroencephalography and clinical neurophysiology.

[62]  G. Potts An ERP index of task relevance evaluation of visual stimuli , 2004, Brain and Cognition.

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

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

[65]  Carmel Mevorach,et al.  Ignoring the Elephant in the Room: A Neural Circuit to Downregulate Salience , 2010, The Journal of Neuroscience.

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

[67]  J. Nigg,et al.  Single dissociation findings of ADHD deficits in vigilance but not anterior or posterior attention systems. , 2006, Neuropsychology.

[68]  A Kok,et al.  Cerebral event-related potentials associated with selective attention to color: developmental changes from childhood to adulthood. , 1998, Psychophysiology.

[69]  Adam Gazzaley,et al.  Neural Suppression of Irrelevant Information Underlies Optimal Working Memory Performance , 2009, The Journal of Neuroscience.

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

[71]  Seppo P. Ahlfors,et al.  Biasing the brain’s attentional set: I. Cue driven deployments of intersensory selective attention , 2005, Experimental Brain Research.

[72]  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.

[73]  R. Zatorre,et al.  Attention to simultaneous unrelated auditory and visual events: behavioral and neural correlates. , 2005, Cerebral cortex.

[74]  William C. Ogden,et al.  Attended and unattended processing modes: The role of set for spatial location , 2014 .

[75]  Michael W. L. Chee,et al.  Functional imaging correlates of impaired distractor suppression following sleep deprivation , 2012, NeuroImage.

[76]  T. Braver,et al.  Explaining the many varieties of working memory variation: Dual mechanisms of cognitive control. , 2007 .

[77]  F. Xavier Castellanos,et al.  Large-scale brain systems in ADHD: beyond the prefrontal–striatal model , 2012, Trends in Cognitive Sciences.

[78]  C. Spence,et al.  Multisensory Integration: Maintaining the Perception of Synchrony , 2003, Current Biology.

[79]  E. Miller,et al.  An integrative theory of prefrontal cortex function. , 2001, Annual review of neuroscience.

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

[81]  A. Gazzaley,et al.  Distinct mechanisms for the impact of distraction and interruption on working memory in aging , 2012, Neurobiology of Aging.

[82]  Robert T. Knight,et al.  Intermodal Auditory, Visual, and Tactile Attention Modulates Early Stages of Neural Processing , 2009, Journal of Cognitive Neuroscience.