Marker-based ballistocardiographic artifact correction improves spike identification in EEG-fMRI of focal epilepsy patients

OBJECTIVES Ballistocardiographic (BCG) artifacts resemble interictal epileptic discharges (IEDs) and can lead to incorrect IED identification in EEG-fMRI. This study investigates IEDs marked in EEGs corrected using information from a moiré phase tracking (MPT) marker. METHODS EEG-fMRI from 18 patients was processed with conventional methods for BCG removal, while 9 patients used a MPT marker. IEDs were marked first without ECG information. In a second review, suspicious IEDs synchronous with the BCG were discarded. After each review, an event-related fMRI analysis was performed on the marked IEDs. RESULTS No difference was found in the proportion of suspicious IEDs in the 2 patient groups. However, the distribution of IED timings was significantly related to the cardiac cycle in 11 of 18 patients recorded without MPT marker, but only 2 of 9 patients with marker. In patients recorded without marker, failing to discard suspicious IEDs led to more inaccurate fMRI maps and more distant activations. CONCLUSIONS BCG artifact correction based on MPT recordings allowed a more straightforward identification of IEDs that did not require ECG information in the large majority of patients. SIGNIFICANCE Marker-based ballistocardiographic artifact correction greatly facilitates the study of the generators of interictal discharges with EEG-fMRI.

[1]  J. R. Baker,et al.  Simultaneous functional magnetic resonance imaging and electrophysiological recording , 1995 .

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

[3]  Andreas Schulze-Bonhage,et al.  Negative BOLD in default-mode structures measured with EEG-MREG is larger in temporal than extra-temporal epileptic spikes , 2014, Front. Neurosci..

[4]  Mark S. Cohen,et al.  Removing ballistocardiogram (BCG) artifact from full-scalp EEG acquired inside the MR scanner with Orthogonal Matching Pursuit (OMP) , 2014, Front. Neurosci..

[5]  Jean Gotman,et al.  EEG‐fMRI of focal epileptic spikes: Analysis with multiple haemodynamic functions and comparison with gadolinium‐enhanced MR angiograms , 2004, Human brain mapping.

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

[7]  Maxim Zaitsev,et al.  Single shot concentric shells trajectories for ultra fast fMRI , 2012, Magnetic resonance in medicine.

[8]  Afraim Salek-Haddadi,et al.  Event-Related fMRI with Simultaneous and Continuous EEG: Description of the Method and Initial Case Report , 2001, NeuroImage.

[9]  Karen J. Mullinger,et al.  Reference layer artefact subtraction (RLAS): A novel method of minimizing EEG artefacts during simultaneous fMRI , 2014, NeuroImage.

[10]  Louis Lemieux,et al.  Classification of EEG abnormalities in partial epilepsy with simultaneous EEG–fMRI recordings , 2014, NeuroImage.

[11]  R. Kreis,et al.  Restoration of electrophysiological signals distorted by inductive effects of magnetic field gradients during MR sequences , 1999, Magnetic resonance in medicine.

[12]  G. Jackson,et al.  How wrong can we be? The effect of inaccurate mark-up of EEG/fMRI studies in epilepsy , 2009, Clinical Neurophysiology.

[13]  Alan C. Evans,et al.  A general statistical analysis for fMRI data , 2000, NeuroImage.

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

[15]  Karen J. Mullinger,et al.  Identifying the sources of the pulse artefact in EEG recordings made inside an MR scanner , 2013, NeuroImage.

[16]  穴見 公隆,et al.  Stepping stone sampling for retrieving artifact-free electroencephalogram during functional magnetic resonance imaging , 2005 .

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

[18]  Sabine Van Huffel,et al.  Removal of BCG artifacts from EEG recordings inside the MR scanner: A comparison of methodological and validation-related aspects , 2010, NeuroImage.

[19]  Ernst Fernando Lopes Da Silva Niedermeyer,et al.  Electroencephalography, basic principles, clinical applications, and related fields , 1982 .

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

[21]  F. Leijten,et al.  EEG-fMRI in the preoperative work-up for epilepsy surgery. , 2007, Brain : a journal of neurology.

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

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

[24]  Andrzej Cichocki,et al.  Removal of ballistocardiogram artifacts from simultaneously recorded EEG and fMRI data using independent component analysis , 2006, IEEE Transactions on Biomedical Engineering.

[25]  Charles T. Hoffman,et al.  Measurement and Reduction of On-Road Brake Drag , 1979 .

[26]  L. Lemieux,et al.  With or without spikes: localization of focal epileptic activity by simultaneous electroencephalography and functional magnetic resonance imaging. , 2011, Brain : a journal of neurology.

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

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

[29]  Maxim Zaitsev,et al.  Ballistocardiographic artifact removal from simultaneous EEG-fMRI using an optical motion-tracking system , 2013, NeuroImage.

[30]  Maxim Zaitsev,et al.  Comparison of optical and MR‐based tracking , 2015, Magnetic resonance in medicine.

[31]  Oliver Speck,et al.  Measurement and Correction of Microscopic Head Motion during Magnetic Resonance Imaging of the Brain , 2012, PloS one.

[32]  Elizabeth B. Liddle,et al.  Motion-related artefacts in EEG predict neuronally plausible patterns of activation in fMRI data , 2012, NeuroImage.

[33]  Jean Gotman,et al.  Combining EEG and fMRI in the study of epileptic discharges , 2011, Epilepsia.

[34]  G. Srivastava,et al.  ICA-based procedures for removing ballistocardiogram artifacts from EEG data acquired in the MRI scanner , 2005, NeuroImage.

[35]  L Bozzao,et al.  Real-time MR artifacts filtering during continuous EEG/fMRI acquisition. , 2003, Magnetic resonance imaging.

[36]  Abraham Z. Snyder,et al.  Moving GLM ballistocardiogram artifact reduction for EEG acquired simultaneously with fMRI , 2007, Clinical Neurophysiology.

[37]  Jürgen Hennig,et al.  Single shot whole brain imaging using spherical stack of spirals trajectories , 2013, NeuroImage.

[38]  Helmut Laufs,et al.  Functional imaging of seizures and epilepsy: evolution from zones to networks. , 2012, Current opinion in neurology.

[39]  J. Hennig,et al.  Three‐dimensional MR‐encephalography: Fast volumetric brain imaging using rosette trajectories , 2011, Magnetic resonance in medicine.

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

[41]  Fernando Lopes da Silva,et al.  Comprar Niedermeyer's Electroencephalography, 6/e (Basic Principles, Clinical Applications, and Related Fields ) | Fernando Lopes Da Silva | 9780781789424 | Lippincott Williams & Wilkins , 2010 .

[42]  Mark W. Woolrich,et al.  Advances in functional and structural MR image analysis and implementation as FSL , 2004, NeuroImage.

[43]  Louis Lemieux,et al.  EEG-fMRI; Physiological Basis, Technique, and Applications , 2010 .

[44]  Gian Luca Romani,et al.  Complete artifact removal for EEG recorded during continuous fMRI using independent component analysis , 2007, NeuroImage.

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

[46]  Christophe Phillips,et al.  Rejection of pulse related artefact (PRA) from continuous electroencephalographic (EEG) time series recorded during functional magnetic resonance imaging (fMRI) using constraint independent component analysis (cICA) , 2009, NeuroImage.

[47]  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.

[48]  Louis Lemieux,et al.  EEG/Functional MRI in Epilepsy: The Queen Square Experience , 2004, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

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

[50]  Jonathan S. Lewin,et al.  Dynamic tracking in interventional MRI using wavelet-encoded gradient-echo sequences , 1998, IEEE Transactions on Medical Imaging.

[51]  G H Glover,et al.  Image‐based method for retrospective correction of physiological motion effects in fMRI: RETROICOR , 2000, Magnetic resonance in medicine.

[52]  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.

[53]  V. Kirsch,et al.  Avoiding the Ballistocardiogram (BCG) Artifact of EEG data acquired simultaneously with fMRI by pulse triggered presentation of stimuli , 2009, NeuroImage.

[54]  Stephan Wolff,et al.  Spatial filters and automated spike detection based on brain topographies improve sensitivity of EEG–fMRI studies in focal epilepsy , 2007, NeuroImage.

[55]  J. Gotman.  Epileptic networks studied with EEG‐fMRI , 2008, Epilepsia.

[56]  Maxim Zaitsev,et al.  Enhancement of temporal resolution and BOLD sensitivity in real-time fMRI using multi-slab echo-volumar imaging , 2012, NeuroImage.