Causality in the Association between P300 and Alpha Event-Related Desynchronization

Recent findings indicated that both P300 and alpha event-related desynchronization (α-ERD) were associated, and similarly involved in cognitive brain functioning, e.g., attention allocation and memory updating. However, an explicit causal influence between the neural generators of P300 and α-ERD has not yet been investigated. In the present study, using an oddball task paradigm, we assessed the task effect (target vs. non-target) on P300 and α-ERD elicited by stimuli of four sensory modalities, i.e., audition, vision, somatosensory, and pain, estimated their respective neural generators, and investigated the information flow among their neural generators using time-varying effective connectivity in the target condition. Across sensory modalities, the scalp topographies of P300 and α-ERD were similar and respectively maximal at parietal and occipital regions in the target condition. Source analysis revealed that P300 and α-ERD were mainly generated from posterior cingulate cortex and occipital lobe respectively. As revealed by time-varying effective connectivity, the cortical information was consistently flowed from α-ERD sources to P300 sources in the target condition for all four sensory modalities. All these findings showed that P300 in the target condition is modulated by the changes of α-ERD, which would be useful to explore neural mechanism of cognitive information processing in the human brain.

[1]  E. Adrian,et al.  THE BERGER RHYTHM: POTENTIAL CHANGES FROM THE OCCIPITAL LOBES IN MAN , 1934 .

[2]  J. S. Barlow,et al.  Rhythmic activity induced by photic stimulation in relation to intrinsic alpha activity of the brain in man. , 1960, Electroencephalography and clinical neurophysiology.

[3]  A. Rémond,et al.  Variations in average visual evoked potential as a function of the alpha rhythm phase ("autostimulation"). , 1967, Electroencephalography and clinical neurophysiology.

[4]  C. Granger Investigating Causal Relations by Econometric Models and Cross-Spectral Methods , 1969 .

[5]  Jorge L. Mendoza,et al.  Analysis of repeated measurements. , 1979 .

[6]  N. Galloway,et al.  Evoked Potentials , 1987 .

[7]  E Başar,et al.  A new approach to endogenous event-related potentials in man: relation between EEG and P300-wave. , 1984, The International journal of neuroscience.

[8]  E. Basar,et al.  Important associations among EEG-dynamics, event-related potentials, short-term memory and learning. , 1985, The International journal of neuroscience.

[9]  M. Alexander,et al.  Principles of Neural Science , 1981 .

[10]  G. Hakerem,et al.  The effect of prestimulus alpha activity on the P300. , 1988, Psychophysiology.

[11]  C. Braun,et al.  Somatosensory event-related potentials to painful and non-painful stimuli: effects of attention , 1989, Pain.

[12]  Ellen R. Girden,et al.  ANOVA: Repeated Measures , 1991 .

[13]  E. Basar,et al.  Sensory and cognitive components of brain resonance responses. An analysis of responsiveness in human and cat brain upon visual and auditory stimulation. , 1991, Acta oto-laryngologica. Supplementum.

[14]  M. Brandt,et al.  The relationship between prestimulus-alpha amplitude and visual evoked potential amplitude. , 1991, The International journal of neuroscience.

[15]  M. Brandt,et al.  The effect of the phase of prestimulus alpha activity on the averaged visual evoked response. , 1991, Electroencephalography and clinical neurophysiology.

[16]  M. Brandt,et al.  Pre-stimulus spectral EEG patterns and the visual evoked response. , 1991, Electroencephalography and clinical neurophysiology.

[17]  E. Basar,et al.  Enhancement of visual evoked potentials by stimulation during low prestimulus EEG stages. , 1993, The International journal of neuroscience.

[18]  E. Basar,et al.  Please Scroll down for Article International Journal of Neuroscience Prestimulus Eeg-activity Strongly Influences the Auditory Evoked Vertex Response: a New Method for Selective Averaging , 2022 .

[19]  G Pfurtscheller,et al.  Event-related desynchronization (ERD) during visual processing. , 1994, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[20]  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.

[21]  J. Polich,et al.  Cognitive and biological determinants of P300: an integrative review , 1995, Biological Psychology.

[22]  S Micheloyannis,et al.  Generators for human P300 elicited by somatosensory stimuli using multiple dipole source analysis , 1996, Neuroscience.

[23]  D. Yarnitsky,et al.  The P300 in pain evoked potentials , 1996, Pain.

[24]  Ulrich Hegerl,et al.  Dipole source analysis of P300 component of the auditory evoked potential: a methodological advance? , 1997, Psychiatry Research: Neuroimaging.

[25]  E. Basar,et al.  Alpha oscillations in brain functioning: an integrative theory. , 1997, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[26]  Juliana Yordanova,et al.  Is the alpha rhythm a control parameter for brain responses? , 1997, Biological Cybernetics.

[27]  F. H. Lopes da Silva,et al.  Alpha rhythms: noise, dynamics and models. , 1997, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[28]  E. Basar,et al.  A possible role of evoked alpha in primary sensory processing: common properties of cat intracranial recordings and human EEG and MEG. , 1997, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[29]  S Makeig,et al.  Blind separation of auditory event-related brain responses into independent components. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[30]  J. Polich,et al.  On the relationship between EEG and P300: individual differences, aging, and ultradian rhythms. , 1997, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[31]  W. Klimesch EEG-alpha rhythms and memory processes. , 1997, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[32]  M. Brandt Visual and auditory evoked phase resetting of the alpha EEG. , 1997, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[33]  W. Klimesch,et al.  Induced alpha band power changes in the human EEG and attention , 1998, Neuroscience Letters.

[34]  J. Yordanova,et al.  Event‐related alpha oscillations are functionally associated with P300 during information processing , 1998, Neuroreport.

[35]  F. L. D. Silva,et al.  Event-related EEG/MEG synchronization and desynchronization: basic principles , 1999, Clinical Neurophysiology.

[36]  E. Basar,et al.  Oscillatory brain theory: a new trend in neuroscience. , 1999, IEEE engineering in medicine and biology magazine : the quarterly magazine of the Engineering in Medicine & Biology Society.

[37]  J. Polich,et al.  P3a and P3b from typical auditory and visual stimuli , 1999, Clinical Neurophysiology.

[38]  M. Schürmann,et al.  Event-related alpha oscillations in task processing , 1999, Clinical Neurophysiology.

[39]  E. Basar,et al.  Brain oscillations in perception and memory. , 2000, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[40]  R. Barry,et al.  EEG alpha activity and the ERP to target stimuli in an auditory oddball paradigm. , 2000, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[41]  E. Basar,et al.  Gamma, alpha, delta, and theta oscillations govern cognitive processes. , 2001, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[42]  M Schürmann,et al.  Functional aspects of alpha oscillations in the EEG. , 2001, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[43]  C. Granger Investigating causal relations by econometric models and cross-spectral methods , 1969 .

[44]  Research tutorial , 2001 .

[45]  Luiz A. Baccalá,et al.  Partial directed coherence: a new concept in neural structure determination , 2001, Biological Cybernetics.

[46]  T. Sejnowski,et al.  Analysis and visualization of single‐trial event‐related potentials , 2001, Human brain mapping.

[47]  J. Polich,et al.  P300 and alpha event-related desynchronization (ERD). , 2001, Psychophysiology.

[48]  S. Schultz Principles of Neural Science, 4th ed. , 2001 .

[49]  M. Bastiaansen,et al.  Event-related alpha and theta responses in a visuo-spatial working memory task , 2002, Clinical Neurophysiology.

[50]  R. Kakigi,et al.  Preferential stimulation of Aδ fibers by intra-epidermal needle electrode in humans , 2002, Pain.

[51]  Luo Chang-qing Simulation and Application of Queue Model , 2002 .

[52]  Mark E Ladd,et al.  Sparse imaging of the auditory oddball task with functional MRI , 2003, Neuroreport.

[53]  U. Baumgärtner,et al.  Clinical usefulness of laser-evoked potentials , 2003, Neurophysiologie Clinique/Clinical Neurophysiology.

[54]  M. Scherg,et al.  Localizing P300 Generators in Visual Target and Distractor Processing: A Combined Event-Related Potential and Functional Magnetic Resonance Imaging Study , 2004, The Journal of Neuroscience.

[55]  R. Barry,et al.  Event-related potentials in the auditory oddball as a function of EEG alpha phase at stimulus onset , 2004, Clinical Neurophysiology.

[56]  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.

[57]  Jaroslaw Zygierewicz,et al.  On the statistical significance of event-related EEG desynchronization and synchronization in the time-frequency plane , 2004, IEEE Transactions on Biomedical Engineering.

[58]  D. Linden The P300: Where in the Brain Is It Produced and What Does It Tell Us? , 2005, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[59]  Matthew J. Brookes,et al.  GLM-beamformer method demonstrates stationary field, alpha ERD and gamma ERS co-localisation with fMRI BOLD response in visual cortex , 2005, NeuroImage.

[60]  William Gaetz,et al.  Localization of sensorimotor cortical rhythms induced by tactile stimulation using spatially filtered MEG , 2006, NeuroImage.

[61]  Andrej Stancák,et al.  Cortical oscillatory changes occurring during somatosensory and thermal stimulation. , 2006, Progress in brain research.

[62]  Koji Inui,et al.  Temporal analysis of cortical mechanisms for pain relief by tactile stimuli in humans. , 2006, Cerebral cortex.

[63]  J. Palva,et al.  New vistas for alpha-frequency band oscillations. , 2007, Trends in neurosciences.

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

[65]  Lihua Mao,et al.  Event-related theta and alpha oscillations mediate empathy for pain , 2008, Brain Research.

[66]  Yong Hu,et al.  fMRI-constrained source analysis of visual P300 in Landolt ring task , 2008 .

[67]  A. Mouraux,et al.  Determinants of laser-evoked EEG responses: pain perception or stimulus saliency? , 2008, Journal of neurophysiology.

[68]  W. Klimesch,et al.  What does phase information of oscillatory brain activity tell us about cognitive processes? , 2008, Neuroscience & Biobehavioral Reviews.

[69]  A Mouraux,et al.  Across-trial averaging of event-related EEG responses and beyond. , 2008, Magnetic resonance imaging.

[70]  C. Rios,et al.  Imaging Alpha Signal Modulation Using an ICA-Based EEG Inverse Approach , 2009 .

[71]  S. A. Hillyard Event-Related Potentials (ERPs) and Cognitive Processing , 2009 .

[72]  Hangyi Jiang,et al.  Mapping of functional areas in the human cortex based on connectivity through association fibers. , 2009, Cerebral cortex.

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

[74]  A. Mouraux,et al.  Low intensity intra-epidermal electrical stimulation can activate Aδ-nociceptors selectively , 2010, PAIN.

[75]  René J. Huster,et al.  The role of the cingulate cortex as neural generator of the N200 and P300 in a tactile response inhibition task , 2010, Human brain mapping.

[76]  Xiaorong Gao,et al.  Spectra-temporal patterns underlying mental addition: An ERP and ERD/ERS study , 2010, Neuroscience Letters.

[77]  Jarmo A. Hämäläinen,et al.  Source localization of event-related potentials to pitch change mapped onto age-appropriate MRIs at 6months of age , 2011, NeuroImage.

[78]  André Mouraux,et al.  Low intensity intra-epidermal electrical stimulation can activate A delta-nociceptors selectively (vol 150, pg 199, 2010) , 2011 .

[79]  Laura Astolfi,et al.  Connectome : A MATLAB toolbox for mapping and imaging of brain , 2010 .

[80]  E. Valentini,et al.  The primary somatosensory cortex largely contributes to the early part of the cortical response elicited by nociceptive stimuli , 2011, NeuroImage.