Dissociable mechanisms supporting awareness: the P300 and gamma in a linguistic attentional blink task.

As demonstrated by the attentional blink (AB) phenomenon, awareness for attended stimuli is governed by sharp capacity limits. We used a linguistic AB task to investigate the neural mechanisms that underlie failures of awareness, examining both event-related potentials and oscillatory brain activity to correctly reported and missed second targets (T2s) presented after a correctly reported first target (T1) in a rapid visual stream of distractors. Correctly reported targets occurring at a short lag (250 ms) after T1-within the classic AB period-elicited enhanced late gamma activity relative to incorrectly reported targets but showed no P300 modulation relative to missed targets. In contrast, correctly reported targets presented at a long lag (830 ms)-outside the classic AB period-elicited a greater P300 component but did not significantly modulate oscillatory activity. This double dissociation suggests that there are multiple neural mechanisms supporting awareness that may operate in parallel. Either the P300 or the gamma can index impairment in the cascade of processing leading to a target's entry into awareness. We conclude that the P300 and gamma activity reflect functionally distinct neural mechanisms, each of which plays an independent role in awareness.

[1]  Alexander Maye,et al.  Temporal dynamics of access to consciousness in the attentional blink , 2007, NeuroImage.

[2]  Pascal Fries,et al.  A Microsaccadic Rhythm Modulates Gamma-Band Synchronization and Behavior , 2009, The Journal of Neuroscience.

[3]  J. Polich,et al.  Neuropsychology and neuropharmacology of P3a and P3b. , 2006, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[4]  J. Changeux,et al.  Experimental and Theoretical Approaches to Conscious Processing , 2011, Neuron.

[5]  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.

[6]  M. Potter,et al.  A two-stage model for multiple target detection in rapid serial visual presentation. , 1995, Journal of experimental psychology. Human perception and performance.

[7]  R. Desimone,et al.  Modulation of Oscillatory Neuronal Synchronization by Selective Visual Attention , 2001, Science.

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

[9]  R. Knight,et al.  Neural origins of the P300. , 2000, Critical reviews in neurobiology.

[10]  G. Humphreys,et al.  Basic processes in reading : visual word recognition , 1993 .

[11]  Guillén Fernández,et al.  Suppression of EEG Gamma Activity May Cause the Attentional Blink , 2002, Consciousness and Cognition.

[12]  R. Heuser Surprise, surprise , 2014, Catheterization and cardiovascular interventions : official journal of the Society for Cardiac Angiography & Interventions.

[13]  S. Hillyard,et al.  Evidence for effects of selective attention in the mid-latency range of the human auditory event-related potential. , 1987, Electroencephalography and clinical neurophysiology. Supplement.

[14]  C S Herrmann,et al.  Magnetoencephalographic responses to illusory figures: early evoked gamma is affected by processing of stimulus features. , 2000, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[15]  Marvin M Chun,et al.  Delayed attentional engagement in the attentional blink. , 2005, Journal of experimental psychology. Human perception and performance.

[16]  E. Basar,et al.  A compound P300-40 Hz response of the cat hippocampus. , 1991 .

[17]  O. Bertrand,et al.  Oscillatory gamma activity in humans and its role in object representation , 1999, Trends in Cognitive Sciences.

[18]  R Dell'Acqua,et al.  Electrophysiological evidence of visual encoding deficits in a cross-modal attentional blink paradigm. , 2003, Psychophysiology.

[19]  I. Fried,et al.  Neural “Ignition”: Enhanced Activation Linked to Perceptual Awareness in Human Ventral Stream Visual Cortex , 2009, Neuron.

[20]  E. Basar,et al.  A compound P300-40 Hz response of the cat hippocampus. , 1991, The International journal of neuroscience.

[21]  D. Broadbent,et al.  From detection to identification: Response to multiple targets in rapid serial visual presentation , 1987, Perception & psychophysics.

[22]  J. Pernier,et al.  Induced gamma-band activity during the delay of a visual short-term memory task in humans. , 1998, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[23]  J. Changeux,et al.  A neuronal network model linking subjective reports and objective physiological data during conscious perception , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[24]  J. H. Neely Semantic priming effects in visual word recognition: A selective review of current findings and theories. , 1991 .

[25]  N. Squires,et al.  Two varieties of long-latency positive waves evoked by unpredictable auditory stimuli in man. , 1975, Electroencephalography and clinical neurophysiology.

[26]  Andreas Keil,et al.  Modulation of induced gamma band responses and phase synchrony in a paired associate learning task in the human EEG , 2001, Neuroscience Letters.

[27]  E. Vogel,et al.  Delayed working memory consolidation during the attentional blink , 2002, Psychonomic bulletin & review.

[28]  Catherine Tallon-Baudry,et al.  Induced γ-Band Activity during the Delay of a Visual Short-Term Memory Task in Humans , 1998, The Journal of Neuroscience.

[29]  S. Uchida,et al.  The relationship between the visually evoked P300 event-related potential and gamma band oscillation in the human medial and basal temporal lobes An electrocorticographic study , 2002, Neuroscience Research.

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

[31]  Piotr Jaskowski,et al.  Evidence for an Integrative Role of P3b in Linking Reaction to Perception , 2005 .

[32]  T. Sejnowski,et al.  Electroencephalographic Brain Dynamics Following Manually Responded Visual Targets , 2004, PLoS biology.

[33]  F. Varela,et al.  Perception's shadow: long-distance synchronization of human brain activity , 1999, Nature.

[34]  T. Demiralp,et al.  Effects of task variables on the amplitude and phase-locking of auditory gamma band responses in human. , 1997, The International journal of neuroscience.

[35]  K. Shapiro,et al.  Attention to visual pattern information produces the attentional blink in rapid serial visual presentation. , 1994, Journal of experimental psychology. Human perception and performance.

[36]  Andreas K. Engel,et al.  Temporal Binding, Binocular Rivalry, and Consciousness , 1999, Consciousness and Cognition.

[37]  K. Reinikainen,et al.  Selective attention enhances the auditory 40-Hz transient response in humans , 1993, Nature.

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

[39]  Axel Mecklinger,et al.  Gamma activity in human EEG is related to highspeed memory comparisons during object selective attention , 2001 .

[40]  P. C. Murphy,et al.  Cerebral Cortex , 2017, Cerebral Cortex.

[41]  Jasna Martinovic,et al.  Induced Gamma-band Activity Elicited by Visual Representation of Unattended Objects , 2009, Journal of Cognitive Neuroscience.

[42]  Sander Martens,et al.  Quick Minds Don't Blink: Electrophysiological Correlates of Individual Differences in Attentional Selection , 2006, Journal of Cognitive Neuroscience.

[43]  Joachim Röschke,et al.  Time course of human 40 Hz EEG activity accompanying P3 responses in an auditory oddball paradigm , 1997, Neuroscience Letters.

[44]  Ian M. Thornton,et al.  Representation of Change: Separate Electrophysiological Markers of Attention, Awareness, and Implicit Processing , 2003, Journal of Cognitive Neuroscience.

[45]  E. Viding,et al.  Load theory of selective attention and cognitive control. , 2004, Journal of experimental psychology. General.

[46]  S. Luck,et al.  Electrophysiological correlates of feature analysis during visual search. , 1994, Psychophysiology.

[47]  R. Dell’Acqua,et al.  The Demonstration of Short-Term Consolidation , 1998, Cognitive Psychology.

[48]  E Hennighausen,et al.  Missed prime words within the attentional blink evoke an N400 semantic priming effect. , 2001, Psychophysiology.

[49]  J. Polich Updating P300: An integrative theory of P3a and P3b , 2007, Clinical Neurophysiology.

[50]  Steven A. Hillyard,et al.  Vertex potentials evoked during auditory signal detection: Relation to decision criteria , 1973 .

[51]  K L Shapiro,et al.  Temporary suppression of visual processing in an RSVP task: an attentional blink? . , 1992, Journal of experimental psychology. Human perception and performance.

[52]  E. Donchin Presidential address, 1980. Surprise!...Surprise? , 1981, Psychophysiology.

[53]  R. Verleger,et al.  P3 latency shifts in the attentional blink: Further evidence for second target processing postponement , 2007, Brain Research.

[54]  R. Oostenveld,et al.  Finding Gamma , 2008, Neuron.

[55]  L. Marshall,et al.  Event-related gamma band activity during passive and active oddball tasks. , 1996, Neuroreport.

[56]  S. Dehaene,et al.  Timing of the brain events underlying access to consciousness during the attentional blink , 2005, Nature Neuroscience.

[57]  Mika Koivisto,et al.  Comparison of event-related potentials in attentional blink and repetition blindness , 2008, Brain Research.

[58]  The relationship between the visually evoked P300 event-related potential and gamma band oscillation in the human medial and basal temporal lobes : an electrocorticographic study , 2002 .

[59]  A. Engel,et al.  Event-related potential correlates of the attentional blink phenomenon. , 2003, Brain research. Cognitive brain research.

[60]  Daniel Gembris,et al.  Top-down attentional processing enhances auditory evoked gamma band activity , 2003, Neuroreport.

[61]  Helen J. Neville,et al.  The Role of Awareness in Semantic and Syntactic Processing: An ERP Attentional Blink Study , 2010, Journal of Cognitive Neuroscience.

[62]  E. Bizzi,et al.  The Cognitive Neurosciences , 1996 .

[63]  A. Labarga,et al.  Gamma band activity in an auditory oddball paradigm studied with the wavelet transform , 2001, Clinical Neurophysiology.

[64]  Andreas K. Engel,et al.  EEG gamma-band activity in rapid serial visual presentation , 2006, Experimental Brain Research.

[65]  E. Donchin,et al.  Is the P300 component a manifestation of context updating? , 1988, Behavioral and Brain Sciences.

[66]  M. Kutas,et al.  Semantic and repetition priming within the attentional blink: An event-related brain potential (ERP) investigation study , 2007, Biological Psychology.

[67]  S. Yuval-Greenberg,et al.  The Broadband-Transient Induced Gamma-Band Response in Scalp EEG Reflects the Execution of Saccades , 2009, Brain Topography.

[68]  L. M. Ward,et al.  Rhythms of Consciousness: Binocular Rivalry Reveals Large-Scale Oscillatory Network Dynamics Mediating Visual Perception , 2009, PloS one.

[69]  Andreas Keil,et al.  Neuronal Synchronization and Selective Color Processing in the Human Brain , 2004, Journal of Cognitive Neuroscience.

[70]  V. Lollo,et al.  Beyond the attentional blink: visual masking by object substitution. , 1998, Journal of experimental psychology. Human perception and performance.

[71]  C. Frith,et al.  The Role of Working Memory in Visual Selective Attention , 2001, Science.

[72]  Livio Narici,et al.  Time dynamics of stimulus- and event-related gamma band activity: contrast-VEPs and the visual P300 in man , 2001, Clinical Neurophysiology.

[73]  C Braun,et al.  Gamma-band MEG activity to coherent motion depends on task-driven attention. , 1999, Neuroreport.

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

[75]  S. Dehaene,et al.  Converging Intracranial Markers of Conscious Access , 2009, PLoS biology.

[76]  J. Wolfe,et al.  What attributes guide the deployment of visual attention and how do they do it? , 2004, Nature Reviews Neuroscience.

[77]  C. S. Green,et al.  Action video game modifies visual selective attention , 2003, Nature.

[78]  Matthias M. Müller,et al.  Visually induced gamma-band responses in human electroencephalographic activity — a link to animal studies , 1996, Experimental Brain Research.

[79]  I. Nelken,et al.  Transient Induced Gamma-Band Response in EEG as a Manifestation of Miniature Saccades , 2008, Neuron.

[80]  N. Suga,et al.  Criticisms of 'Specific long-term memory traces in primary auditory cortex' , 2004, Nature Reviews Neuroscience.

[81]  E. Vogel,et al.  Electrophysiological Evidence for a Postperceptual Locus of Suppression during the Attentional Blink Time-based Attention and the Attentional Blink , 1998 .

[82]  K. Shapiro,et al.  The attentional blink , 1997, Trends in Cognitive Sciences.

[83]  C. Herrmann,et al.  Gamma responses and ERPs in a visual classification task , 1999, Clinical Neurophysiology.