Distributed Cortical Phase Synchronization in the EEG Reveals Parallel Attention and Working Memory Processes Involved in the Attentional Blink.

Attentional blink (AB) describes a visuo-perceptual phenomenon in which the second of 2 targets within a rapid serial visual presentation stream is not detected. There are several cognitive models attempting to explain the fundamentals of this information processing bottleneck. Here, we used electroencephalographic recordings and the analysis of interregional phase synchronization of rhythmical brain activity to investigate the neural bases of the AB. By investigating the time course of interregional phase synchronization separately for trials in which participants failed to report the second target correctly (AB trials) and trials in which no AB occurred, and by clustering interregional connections based on their functional similarity, it was possible to define several distinct cortical networks. Analyzing these networks comprising phase synchronization--over a large spectrum of brain frequencies from theta to gamma activity--it was possible to identify neural correlates for cognitive subfunctions involved in the AB, such as the encoding of targets into working memory, tuning of attentional filters, and the recruitment of general cognitive resources. This parallel activation of functionally distinct neural processes substantiates the eligibility of several cognitive models on the AB.

[1]  M Corbetta,et al.  Preserved speech abilities and compensation following prefrontal damage. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[2]  W. Klimesch,et al.  Oscillatory mechanisms of process binding in memory , 2010, Neuroscience & Biobehavioral Reviews.

[3]  K. Mathewson,et al.  To See or Not to See: Prestimulus α Phase Predicts Visual Awareness , 2009, The Journal of Neuroscience.

[4]  Y. Benjamini,et al.  Controlling the false discovery rate: a practical and powerful approach to multiple testing , 1995 .

[5]  E Donchin,et al.  A new method for off-line removal of ocular artifact. , 1983, Electroencephalography and clinical neurophysiology.

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

[7]  F. Varela,et al.  Measuring phase synchrony in brain signals , 1999, Human brain mapping.

[8]  Howard Bowman,et al.  The Attentional Blink Reveals Serial Working Memory Encoding: Evidence from Virtual and Human Event-related Potentials , 2009, Journal of Cognitive Neuroscience.

[9]  W Singer,et al.  Consciousness and the structure of neuronal representations. , 1998, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[10]  Sebastian Müller,et al.  Alpha entrainment is responsible for the attentional blink phenomenon , 2012, NeuroImage.

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

[12]  T. Braver,et al.  Anterior cingulate cortex and response conflict: effects of frequency, inhibition and errors. , 2001, Cerebral cortex.

[13]  M. Potter,et al.  Unmasking the attentional blink. , 2009, Journal of experimental psychology. Human perception and performance.

[14]  V. Lollo,et al.  Visual search is postponed during the attentional blink until the system is suitably reconfigured. , 2007, Journal of experimental psychology. Human perception and performance.

[15]  M. Nieuwenstein,et al.  The attentional blink provides episodic distinctiveness: sparing at a cost. , 2009, Journal of experimental psychology. Human perception and performance.

[16]  P. Fries.  A mechanism for cognitive dynamics: neuronal communication through neuronal coherence , 2005, Trends in Cognitive Sciences.

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

[18]  Christopher L. Asplund,et al.  A central role for the lateral prefrontal cortex in goal-directed and stimulus-driven attention , 2010, Nature Neuroscience.

[19]  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.

[20]  Simon Hanslmayr,et al.  The role of alpha oscillations in temporal attention , 2011, Brain Research Reviews.

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

[22]  W. Klimesch,et al.  Visual discrimination performance is related to decreased alpha amplitude but increased phase locking , 2005, Neuroscience Letters.

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

[24]  Kimron Shapiro,et al.  Modulation of long-range neural synchrony reflects temporal limitations of visual attention in humans. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

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

[26]  C. Olivers,et al.  A boost and bounce theory of temporal attention. , 2008, Psychological review.

[27]  D. Lehmann,et al.  Low resolution electromagnetic tomography: a new method for localizing electrical activity in the brain. , 1994, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[28]  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.

[29]  W. Klimesch.  EEG alpha and theta oscillations reflect cognitive and memory performance: a review and analysis , 1999, Brain Research Reviews.

[30]  Mark D'Esposito,et al.  Alpha-Band Phase Synchrony Is Related to Activity in the Fronto-Parietal Adaptive Control Network , 2012, The Journal of Neuroscience.

[31]  Joachim Gross,et al.  How the brain blinks: towards a neurocognitive model of the attentional blink , 2006, Psychological research.

[32]  J. Martinerie,et al.  The brainweb: Phase synchronization and large-scale integration , 2001, Nature Reviews Neuroscience.

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

[34]  H. Petsche,et al.  Synchronization between prefrontal and posterior association cortex during human working memory. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

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

[36]  M. Friedman.  The Use of Ranks to Avoid the Assumption of Normality Implicit in the Analysis of Variance , 1937 .

[37]  J. Enns,et al.  The attentional blink: Resource depletion or temporary loss of control? , 2005, Psychological research.

[38]  B. Wyble,et al.  The simultaneous type, serial token model of temporal attention and working memory. , 2007, Psychological review.

[39]  A. Cichocki,et al.  Steady-state visually evoked potentials: Focus on essential paradigms and future perspectives , 2010, Progress in Neurobiology.

[40]  C. Gerloff,et al.  Dissociation of sustained attention from central executive functions: local activity and interregional connectivity in the theta range , 2007, The European journal of neuroscience.

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

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

[43]  M. Corbetta,et al.  Right Hemisphere Dominance during Spatial Selective Attention and Target Detection Occurs Outside the Dorsal Frontoparietal Network , 2010, The Journal of Neuroscience.

[44]  George R. Mangun,et al.  The neuroscience of attention : attentional control and selection , 2012 .

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