Lateralized Suppression of Alpha-Band EEG Activity As a Mechanism of Target Processing

Alpha-band (8–12 Hz) EEG activity has been linked to visual attention since the earliest EEG studies. More recent studies using spatial cuing paradigms have shown that alpha is suppressed over the hemisphere contralateral to a to-be-attended location, suggesting that alpha serves as a mechanism of preparatory attention. Here, we demonstrate that alpha also plays a role in active target processing. EEG activity was recorded from a group of healthy male and female human subjects in two visual search experiments. In addition to alpha activity, we also assessed the N2pc event-related potential component, a lateralized transient EEG response that has been tightly linked with the focusing of attention on visual targets. We found that the visual search targets triggered both an N2pc component and a suppression of alpha-band activity that was greatest over the hemisphere contralateral to the target (which we call “target-elicited lateralized alpha suppression” or TELAS). In Experiment 1, both N2pc and TELAS were observed for targets presented in the lower visual field but were absent for upper-field targets. However, these two lateralized effects had different time courses and they responded differently to manipulations of crowding in Experiment 2. These results indicate that lateralized alpha-band activity is involved in active target processing and is not solely a preparatory mechanism and also that TELAS and N2pc reflect a related but separable neural mechanism of visuospatial attention. SIGNIFICANCE STATEMENT The very first EEG studies demonstrated that alpha-band (8–12 Hz) EEG oscillations are suppressed when people attend to visual information and more recent research has shown that cuing an individual to expect a target at a specific location produces lateralized suppression in the contralateral hemisphere. Therefore, lateralized alpha may serve as a preparatory mechanism. In the present study, we found that a similar lateralized alpha effect is triggered by the appearance of a visual target even though the location could not be anticipated, demonstrating that alpha also serves as an active mechanism of target processing. Moreover, we found that alpha lateralization can be dissociated from other lateralized measures of target selection, indicating that it reflects a distinct mechanism of attention.

[1]  M. A. Goodale,et al.  What is the best fixation target? The effect of target shape on stability of fixational eye movements , 2013, Vision Research.

[2]  H. Berger Über das Elektrenkephalogramm des Menschen , 1938, Archiv für Psychiatrie und Nervenkrankheiten.

[3]  S. Luck,et al.  Bridging the Gap between Monkey Neurophysiology and Human Perception: An Ambiguity Resolution Theory of Visual Selective Attention , 1997, Cognitive Psychology.

[4]  Nicholas Gaspelin,et al.  How to get statistically significant effects in any ERP experiment (and why you shouldn't). , 2017, Psychophysiology.

[5]  Steven J. Luck,et al.  The Allocation of Attention and Working Memory in Visual Crowding , 2015, Journal of Cognitive Neuroscience.

[6]  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.

[7]  Roshan Cools,et al.  Region-specific modulations in oscillatory alpha activity serve to facilitate processing in the visual and auditory modalities , 2014, NeuroImage.

[8]  P. Jolicœur,et al.  Differential engagement of attention and visual working memory in the representation and evaluation of the number of relevant targets and their spatial relations: Evidence from the N2pc and SPCN , 2017, Biological Psychology.

[9]  P. Berg,et al.  Ocular artifacts in EEG and event-related potentials I: Scalp topography , 2005, Brain Topography.

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

[11]  Floris P. de Lange,et al.  Local Entrainment of Alpha Oscillations by Visual Stimuli Causes Cyclic Modulation of Perception , 2014, The Journal of Neuroscience.

[12]  Roshan Cools,et al.  Occipital Alpha and Gamma Oscillations Support Complementary Mechanisms for Processing Stimulus Value Associations , 2018, Journal of Cognitive Neuroscience.

[13]  G Mulder,et al.  Visual spatial attention to stimuli presented on the vertical and horizontal meridian: an ERP study. , 1994, Psychophysiology.

[14]  F. Previc,et al.  Visual search asymmetries in three-dimensional space , 1993, Vision Research.

[15]  Steven J. Luck,et al.  Electrophysiological Correlates of the Focusing of Attention within Complex Visual Scenes: N2pc and Related ERP Components , 2011 .

[16]  P. Cavanagh,et al.  The Spatial Resolution of Visual Attention , 2001, Cognitive Psychology.

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

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

[19]  Hans-Jochen Heinze,et al.  The Neural Site of Attention Matches the Spatial Scale of Perception , 2006, The Journal of Neuroscience.

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

[21]  Pierre Jolicoeur,et al.  Mental Rotation Requires Visual Short-term Memory: Evidence from Human Electric Cortical Activity , 2010, Journal of Cognitive Neuroscience.

[22]  G. Mangun,et al.  Top-down Modulation of Neural Activity in Anticipatory Visual Attention: Control Mechanisms Revealed by Simultaneous EEG-fMRI. , 2014, Cerebral cortex.

[23]  G. Thut,et al.  Mechanisms of selective inhibition in visual spatial attention are indexed by α‐band EEG synchronization , 2007, The European journal of neuroscience.

[24]  Sam M. Doesburg,et al.  Top-down alpha oscillatory network interactions during visuospatial attention orienting , 2016, NeuroImage.

[25]  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.

[26]  Marina Schmid,et al.  An Introduction To The Event Related Potential Technique , 2016 .

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

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

[29]  P. Cavanagh,et al.  Attentional resolution and the locus of visual awareness , 1996, Nature.

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

[31]  S. Brandt,et al.  Dynamic upper and lower visual field preferences within the human dorsal frontoparietal attention network , 2011, Human brain mapping.

[32]  A. Compston The Berger rhythm: potential changes from the occipital lobes in man. , 2010, Brain : a journal of neurology.

[33]  Arnaud Delorme,et al.  Single-Trial Normalization for Event-Related Spectral Decomposition Reduces Sensitivity to Noisy Trials , 2011, Front. Psychology.

[34]  W. Ray,et al.  EEG alpha activity reflects attentional demands, and beta activity reflects emotional and cognitive processes. , 1985, Science.

[35]  Ben M. Crittenden,et al.  Distinct Mechanisms for Distractor Suppression and Target Facilitation , 2016, The Journal of Neuroscience.

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

[37]  Steven J. Luck,et al.  ERPLAB: an open-source toolbox for the analysis of event-related potentials , 2014, Front. Hum. Neurosci..

[38]  F. Previc Functional specialization in the lower and upper visual fields in humans: Its ecological origins and neurophysiological implications , 1990, Behavioral and Brain Sciences.

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

[40]  C. Schroeder,et al.  Neuronal Mechanisms of Cortical Alpha Oscillations in Awake-Behaving Macaques , 2008, The Journal of Neuroscience.

[41]  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.

[42]  D. Pollen,et al.  Alpha Rhythm and Eye Movements in Eidetic Imagery , 1972, Nature.

[43]  Edgar Erdfelder,et al.  G*Power 3: A flexible statistical power analysis program for the social, behavioral, and biomedical sciences , 2007, Behavior research methods.

[44]  John Duncan,et al.  A neural basis for visual search in inferior temporal cortex , 1993, Nature.