Realignment parameter-informed artefact correction for simultaneous EEG–fMRI recordings

In this work we introduce a new algorithm to correct the imaging artefacts in the EEG signal measured during fMRI acquisition. The correction techniques proposed so far cannot optimally represent transitions, i.e. when abrupt changes of the artefact properties due to head movements occur. The algorithm developed here takes the head movement parameters from the fMRI signal into account to calculate adequate EEG artefact templates and subsequently correct the distorted EEG data. The data reported in this work demonstrate that the realignment parameter-informed algorithm outperforms the commonly used moving average algorithm if head movements occur. The superiority is reflected by comparing the residual variance after artefact correction with either method. The residual variance is lower around head-movements that exceed head deflections of about 1 mm when applying the realignment parameter-informed algorithm. Additionally, the signal to noise ratio of a surrogate event-related potential (ERP) increased by 10-40% for head displacements larger than 1 mm. The algorithm developed here is particularly suited for studies where head movements of the subject cannot be prevented as in studies with patients, children, or during sleep. Furthermore, the enhanced signal to noise ratio of a single trial ERP indicates the power of the presented algorithm for single trial ERP-fMRI studies in which EEG signal quality is a critical factor.

[1]  R. Oostenveld,et al.  Frontal theta EEG activity correlates negatively with the default mode network in resting state. , 2008, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[2]  Mark S. Cohen,et al.  Simultaneous EEG and fMRI of the alpha rhythm , 2002, Neuroreport.

[3]  A. Engel,et al.  Single-trial EEG–fMRI reveals the dynamics of cognitive function , 2006, Trends in Cognitive Sciences.

[4]  Graeme D. Jackson,et al.  Measurement and reduction of motion and ballistocardiogram artefacts from simultaneous EEG and fMRI recordings , 2007, NeuroImage.

[5]  Jean Gotman,et al.  The BOLD Response to Interictal Epileptiform Discharges , 2002, NeuroImage.

[6]  Karl J. Friston,et al.  Hemodynamic correlates of epileptiform discharges: An EEG-fMRI study of 63 patients with focal epilepsy , 2006, Brain Research.

[7]  T Landis,et al.  Non-invasive epileptic focus localization using EEG-triggered functional MRI and electromagnetic tomography. , 1998, Electroencephalography and clinical neurophysiology.

[8]  Karl J. Friston,et al.  Movement‐Related effects in fMRI time‐series , 1996, Magnetic resonance in medicine.

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

[10]  Andreas Kleinschmidt,et al.  Recent advances in recording electrophysiological data simultaneously with magnetic resonance imaging , 2008, NeuroImage.

[11]  Karen J Mullinger,et al.  Improved artifact correction for combined electroencephalography/functional MRI by means of synchronization and use of vectorcardiogram recordings , 2008, Journal of magnetic resonance imaging : JMRI.

[12]  M. Czisch,et al.  Brain activation and hypothalamic functional connectivity during human non-rapid eye movement sleep: an EEG/fMRI study. , 2006, Brain : a journal of neurology.

[13]  J. Gotman,et al.  Quality of EEG in simultaneous EEG-fMRI for epilepsy , 2003, Clinical Neurophysiology.

[14]  M R Symms,et al.  EEG-triggered functional MRI of interictal epileptiform activity in patients with partial seizures. , 1999, Brain : a journal of neurology.

[15]  Christian Kaufmann,et al.  Altered Processing of Acoustic Stimuli during Sleep: Reduced Auditory Activation and Visual Deactivation Detected by a Combined fMRI/EEG Study , 2002, NeuroImage.

[16]  Christian Seifert,et al.  Single-trial coupling of EEG and fMRI reveals the involvement of early anterior cingulate cortex activation in effortful decision making , 2008, NeuroImage.

[17]  J Sijbers,et al.  Restoration of MR-induced artifacts in simultaneously recorded MR/EEG data. , 1999, Magnetic resonance imaging.

[18]  K J Werhahn,et al.  Electroencephalography during functional echo‐planar imaging: Detection of epileptic spikes using post‐processing methods , 2000, Magnetic resonance in medicine.

[19]  Louis Lemieux,et al.  Identification of EEG Events in the MR Scanner: The Problem of Pulse Artifact and a Method for Its Subtraction , 1998, NeuroImage.

[20]  Emery N. Brown,et al.  Motion and Ballistocardiogram Artifact Removal for Interleaved Recording of EEG and EPs during MRI , 2002, NeuroImage.

[21]  Fernando Henrique Lopes da Silva,et al.  The hemodynamic response of the alpha rhythm: An EEG/fMRI study , 2007, NeuroImage.

[22]  Andreas Kleinschmidt,et al.  EEG-correlated fMRI of human alpha activity , 2003, NeuroImage.

[23]  L. Lemieux,et al.  Recording of EEG during fMRI experiments: Patient safety , 1997, Magnetic resonance in medicine.

[24]  Hellmuth Obrig,et al.  Correlates of alpha rhythm in functional magnetic resonance imaging and near infrared spectroscopy , 2003, NeuroImage.

[25]  Frédéric Grouiller,et al.  A comparative study of different artefact removal algorithms for EEG signals acquired during functional MRI , 2007, NeuroImage.

[26]  S. Debener,et al.  Effects of simultaneous EEG recording on MRI data quality at 1.5, 3 and 7 tesla. , 2008, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

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

[28]  M R Symms,et al.  Methodology: EEG-correlated fMRI. , 2000, Advances in neurology.

[29]  Arno Villringer,et al.  Evaluating gradient artifact correction of EEG data acquired simultaneously with fMRI. , 2007, Magnetic resonance imaging.

[30]  M R Symms,et al.  Spatio-temporal imaging of focal interictal epileptiform activity using EEG-triggered functional MRI. , 2001, Epileptic disorders : international epilepsy journal with videotape.

[31]  Daniel Brandeis,et al.  Synchronization facilitates removal of MRI artefacts from concurrent EEG recordings and increases usable bandwidth , 2006, NeuroImage.

[32]  Robert Turner,et al.  A Method for Removing Imaging Artifact from Continuous EEG Recorded during Functional MRI , 2000, NeuroImage.

[33]  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.

[34]  J. Gotman,et al.  Combining EEG and fMRI in Epilepsy: Methodological Challenges and Clinical Results , 2004, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[35]  Rami K. Niazy,et al.  Removal of FMRI environment artifacts from EEG data using optimal basis sets , 2005, NeuroImage.

[36]  J R Ives,et al.  EEG-triggered echo-planar functional MRI in epilepsy , 1996, Neurology.

[37]  Bettina Sorger,et al.  Improved quality of auditory event-related potentials recorded simultaneously with 3-T fMRI: Removal of the ballistocardiogram artefact , 2007, NeuroImage.

[38]  Daniel Brandeis,et al.  Impaired semantic processing during sentence reading in children with dyslexia: Combined fMRI and ERP evidence , 2008, NeuroImage.

[39]  J. C. de Munck,et al.  Artifact removal in co-registered EEG/fMRI by selective average subtraction , 2007, Clinical Neurophysiology.

[40]  A. Villringer,et al.  Rolandic alpha and beta EEG rhythms' strengths are inversely related to fMRI‐BOLD signal in primary somatosensory and motor cortex , 2009, Human brain mapping.

[41]  S Warach,et al.  Monitoring the patient's EEG during echo planar MRI. , 1993, Electroencephalography and clinical neurophysiology.

[42]  M. Fukunaga,et al.  Low frequency BOLD fluctuations during resting wakefulness and light sleep: A simultaneous EEG‐fMRI study , 2008, Human brain mapping.

[43]  Masato Yumoto,et al.  Stepping stone sampling for retrieving artifact-free electroencephalogram during functional magnetic resonance imaging , 2003, NeuroImage.

[44]  Michiro Negishi,et al.  Removal of time-varying gradient artifacts from EEG data acquired during continuous fMRI , 2004, Clinical Neurophysiology.

[45]  M. Corbetta,et al.  Electrophysiological signatures of resting state networks in the human brain , 2007, Proceedings of the National Academy of Sciences.

[46]  J. Gotman,et al.  Combining EEG and fMRI: A multimodal tool for epilepsy research , 2006, Journal of magnetic resonance imaging : JMRI.