A modified oddball paradigm for investigation of neural correlates of attention: a simultaneous ERP–fMRI study

IntroductionThe objective of the presented study was to develop and evaluate a P300 experimental protocol for simultaneous registration of event-related potentials (ERPs) and functional MRI (fMRI) data with continuous imaging. It may be useful for investigating attention and working memory processes in specific populations, such as children and neuropsychiatric patients.Materials and methodsEleven children were investigated with simultaneous ERP–fMRI. To fulfill requirements of both BOLD and electroencephalographic signal registration, a modified oddball task was used. To verify the ERP–fMRI protocol we also performed a study outside the scanner using a typical two-stimuli oddball paradigm.ResultsLocalization of the P300 component of ERPs partially corresponded with fMRI results in the frontal and parietal brain regions. FMRI activations were found in: middle frontal gyrus, insula, SMA, parietal lobule, thalamus, and cerebellum. Our modified oddball task provided ERP–fMRI results with high level of significance (EEG SNR = 35, fMRI p < 0.05–Bonf.). ERPs obtained in the scanner were comparable with those registered outside the scanner, although some differences in the amplitude were noticed, mainly in the N100 component.ConclusionIn our opinion the presented paradigm may be successfully applied for simultaneous ERP–fMRI registration of neural correlates of attention in vulnerable populations.

[1]  E. John,et al.  Evoked-Potential Correlates of Stimulus Uncertainty , 1965, Science.

[2]  R. C. Oldfield.  The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[3]  R. Hockey.  Stress and fatigue in human performance , 1984 .

[4]  J. Nedzelski.  Advances in Audiology , 1985 .

[5]  P. Ullsperger,et al.  The P300 component of the event-related brain potential and mental effort. , 1988, Ergonomics.

[6]  D. Tank,et al.  Brain magnetic resonance imaging with contrast dependent on blood oxygenation. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[7]  G. Romani,et al.  Auditory evoked magnetic fields and electric potentials , 1990 .

[8]  S. Ogawa.  Brain magnetic resonance imaging with contrast-dependent oxygenation , 1990 .

[9]  M. Scherg.  Fundamentals if dipole source potential analysis , 1990 .

[10]  Gavin S. Lew,et al.  P300, habituation, and response mode , 1993, Physiology & Behavior.

[11]  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.

[12]  P. Berg,et al.  A fast method for forward computation of multiple-shell spherical head models. , 1994, Electroencephalography and clinical neurophysiology.

[13]  John Polich,et al.  P3(00) habituation from auditory and visual stimuli , 1996, Physiology & Behavior.

[14]  Karl J. Friston,et al.  The Role of the Thalamus in “Top Down” Modulation of Attention to Sound , 1996, NeuroImage.

[15]  R T Knight,et al.  Anatomic bases of event-related potentials and their relationship to novelty detection in humans. , 1998, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[16]  J. Polich,et al.  Habituation of P300 from visual stimuli. , 1998, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[17]  A Kok,et al.  Varieties of inhibition: manifestations in cognition, event-related potentials and aging. , 1999, Acta psychologica.

[18]  G. Glover.  Deconvolution of Impulse Response in Event-Related BOLD fMRI1 , 1999, NeuroImage.

[19]  A. Kok.  On the utility of P3 amplitude as a measure of processing capacity. , 2001, Psychophysiology.

[20]  Risto Näätänen,et al.  Effects of Acoustic Gradient Noise from Functional Magnetic Resonance Imaging on Auditory Processing as Reflected by Event-Related Brain Potentials , 2001, NeuroImage.

[21]  N. Logothetis,et al.  Neurophysiological investigation of the basis of the fMRI signal , 2001, Nature.

[22]  Joy Hirsch,et al.  Interconnected Large-Scale Systems for Three Fundamental Cognitive Tasks Revealed by Functional MRI , 2001, Journal of Cognitive Neuroscience.

[23]  Hannu J. Aronen,et al.  Working Memory of Identification of Emotional Vocal Expressions: An fMRI Study , 2001, NeuroImage.

[24]  U Hegerl,et al.  Simultaneous ERP and event-related fMRI: focus on the time course of brain activity in target detection. , 2002, Methods and findings in experimental and clinical pharmacology.

[25]  R. Luthringer,et al.  Planning of pharmacodynamic trials: I. Specificity and possible solutions. II. Stability considerations under placebo and interpretation of drug effects on EEG. , 2002, Methods and findings in experimental and clinical pharmacology.

[26]  P. Skudlarski,et al.  Correlations and dissociations between BOLD signal and P300 amplitude in an auditory oddball task: a parametric approach to combining fMRI and ERP. , 2002, Magnetic resonance imaging.

[27]  M. Brázdil,et al.  A SEEG study of ERP in motor and premotor cortices and in the basal ganglia , 2003, Clinical Neurophysiology.

[28]  Hannu J. Aronen,et al.  Effects of noise from functional magnetic resonance imaging on auditory event-related potentials in working memory task , 2003, NeuroImage.

[29]  Jeffrey R. Binder,et al.  Simultaneous ERP and fMRI of the auditory cortex in a passive oddball paradigm , 2003, NeuroImage.

[30]  E. Darcy Burgund,et al.  Comparison of functional activation foci in children and adults using a common stereotactic space , 2003, NeuroImage.

[31]  Hubertus Maximilian Mehdorn,et al.  Does the cerebellum contribute to specific aspects of attention? , 2003, Neuropsychologia.

[32]  Hoi-Chung Leung,et al.  Frontal activations associated with accessing and evaluating information in working memory: an fMRI study , 2003, NeuroImage.

[33]  M. Murray,et al.  EEG source imaging , 2004, Clinical Neurophysiology.

[34]  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.

[35]  Manuel Abbafati,et al.  Simultaneous EEG-fMRI acquisition: how far is it from being a standardized technique? , 2004, Magnetic resonance imaging.

[36]  Bradley G. Goodyear,et al.  Simultaneous 3-T fMRI and high-density recording of human auditory evoked potentials , 2004, NeuroImage.

[37]  Rainer Goebel,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.

[38]  Nikos K Logothetis,et al.  On the nature of the BOLD fMRI contrast mechanism. , 2004, Magnetic resonance imaging.

[39]  Robert Schmitt,et al.  Integration of fMRI and simultaneous EEG: towards a comprehensive understanding of localization and time-course of brain activity in target detection , 2004, NeuroImage.

[40]  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.

[41]  Kenneth Hugdahl,et al.  Assessing the spatiotemporal evolution of neuronal activation with single-trial event-related potentials and functional MRI. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[42]  P. Berg,et al.  Use of prior knowledge in brain electromagnetic source analysis , 2005, Brain Topography.

[43]  D Gounot,et al.  P300 recordings during event-related fMRI: a feasibility study. , 2005, Brain research. Cognitive brain research.

[44]  Godfrey Pearlson,et al.  An adaptive reflexive processing model of neurocognitive function: supporting evidence from a large scale (n = 100) fMRI study of an auditory oddball task , 2005, NeuroImage.

[45]  Marta Kutas,et al.  Interpreting event-related brain potential (ERP) distributions: Implications of baseline potentials and variability with application to amplitude normalization by vector scaling , 2006, Biological Psychology.

[46]  Natasha M. Maurits,et al.  Correlating the alpha rhythm to BOLD using simultaneous EEG/fMRI: Inter-subject variability , 2006, NeuroImage.

[47]  Peter Stoeter,et al.  Distributed BOLD-response in association cortex vector state space predicts reaction time during selective attention , 2006, NeuroImage.

[48]  S. Galderisi,et al.  The cortical generators of P3a and P3b: A LORETA study , 2007, Brain Research Bulletin.

[49]  M. Roth,et al.  Single‐trial analysis of oddball event‐related potentials in simultaneous EEG‐fMRI , 2007, Human brain mapping.

[50]  Mark A Elliott,et al.  Hemodynamic responses in neural circuitries for detection of visual target and novelty: An event‐related fMRI study , 2007, Human brain mapping.

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

[52]  S. Debener,et al.  Simultaneous recording of EEG and BOLD responses: a historical perspective. , 2008, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[53]  Bart Vanrumste,et al.  Journal of Neuroengineering and Rehabilitation Open Access Review on Solving the Inverse Problem in Eeg Source Analysis , 2022 .

[54]  M. Catani,et al.  A diffusion tensor imaging tractography atlas for virtual in vivo dissections , 2008, Cortex.

[55]  S. Debener,et al.  Properties of the ballistocardiogram artefact as revealed by EEG recordings at 1.5, 3 and 7 T static magnetic field strength. , 2008, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[56]  Bettina Sorger,et al.  Novelty and target processing during an auditory novelty oddball: A simultaneous event-related potential and functional magnetic resonance imaging study , 2008, NeuroImage.

[57]  Siamak Shahidi,et al.  BRAIN RES BULL , 2008 .

[58]  Jessica A. Grahn,et al.  The cognitive functions of the caudate nucleus , 2008, Progress in Neurobiology.

[59]  David Friedman,et al.  Single-trial discrimination for integrating simultaneous EEG and fMRI: Identifying cortical areas contributing to trial-to-trial variability in the auditory oddball task , 2009, NeuroImage.

[60]  Kenneth Hugdahl,et al.  Identification of attention and cognitive control networks in a parametric auditory fMRI study , 2010, Neuropsychologia.

[61]  Lee M. Miller,et al.  Auditory attentional control and selection during cocktail party listening. , 2010, Cerebral cortex.

[62]  P. Bogorodzki,et al.  Changes in fMRI BOLD response to increasing and decreasing task difficulty during auditory perception of temporal order , 2010, Neurobiology of Learning and Memory.

[63]  A. Kübler,et al.  Motivation modulates the P300 amplitude during brain–computer interface use , 2010, Clinical Neurophysiology.

[64]  T. Robbins,et al.  Abnormal structure of frontostriatal brain systems is associated with aspects of impulsivity and compulsivity in cocaine dependence , 2011, Brain : a journal of neurology.

[65]  B. Balleine,et al.  Annals of the New York Academy of Sciences the Orbitofrontal Cortex, Predicted Value, and Choice , 2022 .

[66]  Karsten Specht,et al.  Attention and cognitive control networks assessed in a dichotic listening fMRI study , 2011, Brain and Cognition.

[67]  M. Shapiro,et al.  The orbitofrontal cortex and response selection , 2011, Annals of the New York Academy of Sciences.

[68]  Jane E. Joseph,et al.  Prefrontal cortex and drug abuse vulnerability: Translation to prevention and treatment interventions , 2011, Brain Research Reviews.

[69]  Richard G. Wise,et al.  Separating neural and vascular effects of caffeine using simultaneous EEG–FMRI: Differential effects of caffeine on cognitive and sensorimotor brain responses , 2012, NeuroImage.

[70]  Einat Liebenthal,et al.  Within-subject joint independent component analysis of simultaneous fMRI/ERP in an auditory oddball paradigm , 2012, NeuroImage.

[71]  R. O’Connell,et al.  A simultaneous ERP/fMRI investigation of the P300 aging effect , 2012, Neurobiology of Aging.