Simultaneously recorded EEG–fMRI: Removal of gradient artifacts by subtraction of head movement related average artifact waveforms

Electroencephalograms (EEGs) recorded simultaneously with functional magnetic resonance imaging (fMRI) are corrupted by large repetitive artifacts generated by the switched MR gradients. Several methods have been proposed to remove these distortions by subtraction of averaged artifact templates from the ongoing EEG. Here, we present a modification of this approach which accounts for head movements to improve the extracted template. Using the fMRI analysis package statistical parametric mapping (SPM; FIL London) the head displacement is determined at each half fMRI‐volume. The basic idea is to apply a moving average algorithm for template extraction but to include only epochs that were obtained at the same head position as the artefact to be removed. This approach was derived from phantom EEG measurements demonstrating substantial variations of the artefact waveform in response to movements of the phantom in the MRI magnet. To further reduce the residual noise, we applied a resampling algorithm which aligns the EEG samples in a strict adaptive manner to the fMRI timing. Finally, we propose a new algorithm to suppress residual artifacts such as those occasionally observed in case of brief strong movements, which are not reflected by the movement indicator because of the limited temporal resolution of the fMRI sequence. On the basis of EEG recordings of six subjects these measures combined reduce the residual artefact activity quantified in terms of the spectral power at the gradient repetition rate and its harmonics by roughly 20 to 50% (depending on the amount of movement) predominantly in frequencies beyond 30 Hz. Hum Brain Mapp, 2009. © 2009 Wiley‐Liss, Inc.

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

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

[3]  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.

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

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

[6]  Nikos K Logothetis,et al.  Simultaneous EEG and fMRI in the macaque monkey at 4.7 Tesla. , 2005, Magnetic resonance imaging.

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

[8]  Kazuki Iwata,et al.  Artifact reduction for simultaneous EEG/fMRI recording: Adaptive FIR reduction of imaging artifacts , 2006, Clinical Neurophysiology.

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

[10]  Arno Villringer,et al.  Visual evoked potentials recovered from fMRI scan periods , 2005, Human brain mapping.

[11]  M. Verhoye,et al.  Reduction of ECG and gradient related artifacts in simultaneously recorded human EEG/MRI data. , 2000, Magnetic resonance imaging.

[12]  Mark S. Cohen,et al.  Simultaneous EEG and fMRI made easy , 2001, NeuroImage.

[13]  Gian Luca Romani,et al.  Complete artifact removal for EEG recorded during continuous fMRI using independent component analysis , 2007, 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]  Mark S. Cohen,et al.  Acquiring simultaneous EEG and functional MRI , 2000, Clinical Neurophysiology.

[16]  F Kruggel,et al.  Recording of the event‐related potentials during functional MRI at 3.0 Tesla field strength , 2000, Magnetic resonance in medicine.

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

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

[19]  N. Thakor,et al.  Removal of ECG interference from the EEG recordings in small animals using independent component analysis , 2001, Journal of Neuroscience Methods.

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

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

[22]  Tömme Noesselt,et al.  Endoscopic eye tracking system for fMRI , 2007, Journal of Neuroscience Methods.

[23]  J.P.A. Kuijer,et al.  Correction for desynchronization of EEG and fMRI clocks through data interpolation optimizes artifact reduction , 2007, 2007 29th Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

[24]  P. Welch The use of fast Fourier transform for the estimation of power spectra: A method based on time averaging over short, modified periodograms , 1967 .

[25]  O. Speck,et al.  Prospective Real-Time Slice-by-Slice Motion Correction for fMRI in Freely Moving Subjects , 2006, Magnetic Resonance Materials in Physics, Biology and Medicine.

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