Theta Oscillation Reveals the Temporal Involvement of Different Attentional Networks in Contingent Reorienting

In the visual world, rapidly reorienting to relevant objects outside the focus of attention is vital for survival. This ability from the interaction between goal-directed and stimulus-driven attentional control is termed contingent reorienting. Neuroimaging studies have demonstrated activations of the ventral and dorsal attentional networks (DANs) which exhibit right hemisphere dominance, but the temporal dynamics of the attentional networks still remain unclear. The present study used event-related potential (ERP) to index the locus of spatial attention and Hilbert-Huang transform (HHT) to acquire the time-frequency information during contingent reorienting. The ERP results showed contingent reorienting induced significant N2pc on both hemispheres. In contrast, our time-frequency analysis found further that, unlike the N2pc, theta oscillation during contingent reorienting differed between hemispheres and experimental sessions. The inter-trial coherence (ITC) of the theta oscillation demonstrated that the two sides of the attentional networks became phase-locked to contingent reorienting at different stages. The left attentional networks were associated with contingent reorienting in the first experimental session whereas the bilateral attentional networks play a more important role in this process in the subsequent session. This phase-locked information suggests a dynamic temporal evolution of the involvement of different attentional networks in contingent reorienting and a potential role of the left ventral network in the first session.

[1]  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.

[2]  Bryan R. Burnham,et al.  The visual hemifield asymmetry in the spatial blink during singleton search and feature search , 2011, Brain and Cognition.

[3]  C. Miniussi,et al.  New insights into rhythmic brain activity from TMS–EEG studies , 2009, Trends in Cognitive Sciences.

[4]  P. König,et al.  Top-down processing mediated by interareal synchronization. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[5]  R. VanRullen,et al.  The Phase of Ongoing Oscillations Mediates the Causal Relation between Brain Excitation and Visual Perception , 2011, The Journal of Neuroscience.

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

[7]  Steven Yantis,et al.  Stimulus-Driven and Goal-Directed Attentional Control , 2002 .

[8]  Steven J Luck,et al.  Active suppression of distractors that match the contents of visual working memory , 2011, Visual cognition.

[9]  Michael Zehetleitner,et al.  Top-down control of attention: it's gradual, practice-dependent, and hierarchically organized. , 2012, Journal of experimental psychology. Human perception and performance.

[10]  Dominique Lamy,et al.  Effects of task relevance and stimulus-driven salience in feature-search mode. , 2004, Journal of experimental psychology. Human perception and performance.

[11]  Steven J Luck,et al.  Capture versus suppression of attention by salient singletons: Electrophysiological evidence for an automatic attend-to-me signal , 2010, Attention, perception & psychophysics.

[12]  W. Drongelen,et al.  Localization of brain electrical activity via linearly constrained minimum variance spatial filtering , 1997, IEEE Transactions on Biomedical Engineering.

[13]  Hong Bao,et al.  GPGPU-Aided Ensemble Empirical-Mode Decomposition for EEG Analysis During Anesthesia , 2010, IEEE Transactions on Information Technology in Biomedicine.

[14]  A. Nobre.  The attentive homunculus: Now you see it, now you don't , 2001, Neuroscience & Biobehavioral Reviews.

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

[16]  Susan L. Travis,et al.  Neural Responses to Target Features outside a Search Array Are Enhanced during Conjunction but Not Unique-Feature Search , 2014, The Journal of Neuroscience.

[17]  M. Rushworth,et al.  TMS in the parietal cortex: Updating representations for attention and action , 2006, Neuropsychologia.

[18]  Slawomir J. Nasuto,et al.  Evaluation of Empirical Mode Decomposition for Event-Related Potential Analysis , 2011, EURASIP J. Adv. Signal Process..

[19]  Hualou Liang,et al.  Empirical mode decomposition: a method for analyzing neural data , 2005, Neurocomputing.

[20]  Stephen J. Gotts,et al.  Cell-Type-Specific Synchronization of Neural Activity in FEF with V 4 during Attention , 2022 .

[21]  Charles M. Gaona,et al.  Frequency-specific mechanism links human brain networks for spatial attention , 2013, Proceedings of the National Academy of Sciences.

[22]  Andrew B. Leber,et al.  Coordination of Voluntary and Stimulus-Driven Attentional Control in Human Cortex , 2005, Psychological science.

[23]  Aurelie L. Manuel,et al.  Task relevance effects in electrophysiological brain activity: Early, but not first , 2014, NeuroImage.

[24]  J. C. Johnston,et al.  Involuntary covert orienting is contingent on attentional control settings. , 1992, Journal of experimental psychology. Human perception and performance.

[25]  Nicholas E. DiQuattro,et al.  Effective connectivity during feature-based attentional capture: evidence against the attentional reorienting hypothesis of TPJ. , 2014, Cerebral cortex.

[26]  C. Stam,et al.  Nonlinear dynamical analysis of EEG and MEG: Review of an emerging field , 2005, Clinical Neurophysiology.

[27]  R. Desimone,et al.  High-Frequency, Long-Range Coupling Between Prefrontal and Visual Cortex During Attention , 2009, Science.

[28]  N. Yeung,et al.  The roles of cortical oscillations in sustained attention , 2015, Trends in Cognitive Sciences.

[29]  Stephen J. Gotts,et al.  Cell-Type-Specific Synchronization of Neural Activity in FEF with V4 during Attention , 2012, Neuron.

[30]  David Poeppel,et al.  Asymptotic SNR of scalar and vector minimum-variance beamformers for neuromagnetic source reconstruction , 2004, IEEE Transactions on Biomedical Engineering.

[31]  N. Huang,et al.  The empirical mode decomposition and the Hilbert spectrum for nonlinear and non-stationary time series analysis , 1998, Proceedings of the Royal Society of London. Series A: Mathematical, Physical and Engineering Sciences.

[32]  C. van Vreeswijk,et al.  What Is the Neural Code , 2006 .

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

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

[35]  Marta Kutas,et al.  Mass univariate analysis of event-related brain potentials/fields II: Simulation studies. , 2011, Psychophysiology.

[36]  W. Singer,et al.  Dynamic predictions: Oscillations and synchrony in top–down processing , 2001, Nature Reviews Neuroscience.

[37]  Gabriel Rilling,et al.  Empirical mode decomposition as a filter bank , 2004, IEEE Signal Processing Letters.

[38]  J. Lisman,et al.  The Theta-Gamma Neural Code , 2013, Neuron.

[39]  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.

[40]  J. Theeuwes.  Top-down and bottom-up control of visual selection. , 2010, Acta psychologica.

[41]  G. Buzsáki,et al.  Neuronal Oscillations in Cortical Networks , 2004, Science.

[42]  Andrew B. Leber,et al.  Made you blink! Contingent attentional capture produces a spatial blink , 2002, Perception & psychophysics.

[43]  M. Corbetta,et al.  Interaction of Stimulus-Driven Reorienting and Expectation in Ventral and Dorsal Frontoparietal and Basal Ganglia-Cortical Networks , 2009, The Journal of Neuroscience.

[44]  Jason G. Goldman,et al.  Top-down control. , 2014, Scientific American.

[45]  S. Yantis,et al.  Transient neural activity in human parietal cortex during spatial attention shifts , 2002, Nature Neuroscience.

[46]  Antígona Martínez,et al.  Spatial attention boosts short-latency neural responses in human visual cortex , 2012, NeuroImage.

[47]  R. Abrams,et al.  Visual field asymmetry in attentional capture , 2010, Brain and Cognition.

[48]  Wei-Kuang Liang,et al.  An improved method for measuring mismatch negativity using ensemble empirical mode decomposition , 2016, Journal of Neuroscience Methods.

[49]  Robert Oostenveld,et al.  Imaging the human motor system’s beta-band synchronization during isometric contraction , 2008, NeuroImage.

[50]  N. Huang,et al.  The Mechanism for Frequency Downshift in Nonlinear Wave Evolution , 1996 .

[51]  O. Tzeng,et al.  Right temporoparietal junction and attentional reorienting , 2013, Human brain mapping.

[52]  Norden E. Huang,et al.  A review on Hilbert‐Huang transform: Method and its applications to geophysical studies , 2008 .

[53]  Addie Johnson,et al.  The P4pc: an electrophysiological marker of attentional disengagement? , 2011, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

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

[55]  Geoffrey F Woodman,et al.  Serial deployment of attention during visual search. , 2003, Journal of experimental psychology. Human perception and performance.

[56]  Artur Luczak,et al.  Temporal variability of the N2pc during efficient and inefficient visual search , 2012, Neuropsychologia.

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

[58]  M. Corbetta,et al.  The Reorienting System of the Human Brain: From Environment to Theory of Mind , 2008, Neuron.

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

[60]  Anders Petersen,et al.  Attentional Capture by Salient Distractors during Visual Search Is Determined by Temporal Task Demands , 2012, Journal of Cognitive Neuroscience.