Electroencephalography During Functional Echo-Planar Imaging: Detection of Epileptic Spikes Using Post-processing Methods

Transcription

1 Magnetic Resonance in Medicine 44: (2000) Electroencephalography During Functional Echo-Planar Imaging: Detection of Epileptic Spikes Using Post-processing Methods A. Hoffmann, 1 * L. Jäger, 1 K.J. Werhahn, 2 M. Jaschke, 3 S. Noachtar, 2 and M. Reiser 1 EEG has been used to trigger functional MRI of patients with focal epilepsy, but EEG can be obscured by artifacts during MR data acquisition, and no continuous correlation of EEG and MRI has been possible without limiting the image time. Artifacts caused by an MRI sequence were investigated in five healthy subjects, and an EEG of five patients with epileptic discharges was recorded during echo-planar imaging. All interfering frequencies in the EEG were discrete and defined by loop structures in the MRI sequence. In post-processing of the EEG interfering frequencies were automatically detected by comparing the frequency spectra of the EEG recorded before and during imaging. After elimination of interfering frequencies by filters in the time domain or by Fourier transform, reliable spike detection in the EEG recorded during MR data acquisition became feasible, without loss of EEG quality. Magn Reson Med 44: , Wiley-Liss, Inc. Key words: EEG; fmri; epilepsy; epileptic spike; filtering 1 Institute of Diagnostic Radiology, Klinikum Grosshadern, University of Munich, Munich, Germany. 2 Department of Neurology, Klinikum Grosshadern, University of Munich, Munich, Germany. 3 Schwarzer Ltd., Munich, Germany. *Correspondence to: Alexander Hoffmann, Institute of Diagnostic Radiology, Klinikum Grosshadern, Marchioninistr. 15, Munich, Germany. alexander.hoffmann@ikra.med.uni-muenchen.de Received 10 December 1999; revised 8 May 2000; accepted 21 June Wiley-Liss, Inc. 791 Electroencephalography (EEG) within an MR imager can be used to trigger functional MRI (fmri) in relation to electrical brain activity. The most promising application of EEG-triggered fmri is as a noninvasive way to localize interictal activity in epilepsy (1 3). It has been shown that EEG recordings in the MRI scanner are possible without loss of MR image quality (4,5). Artifacts in the EEG synchronous with the electrocardiogram (ECG) have been observed in the static magnetic field (6 9), and solutions to subtract these artifacts have been presented (6,7,9). However, during MR data acquisition the EEG was always completely covered by interference (2 5,7 9), and EEG analysis was only possible before and after MRI activity. The onset of the blood oxygenation level dependent (BOLD) contrast (10) used for fmri starts 3 sec after a given event in the EEG and stays active for up to 10 sec (11,12). To exclude the influence of any further undetectable EEG events during MRI on the image contrast, imaging must start about 3 sec after the event (when the BOLD contrast starts) and must be finished after a further 3 sec (when the BOLD contrast of unwanted events during the scan starts). Therefore, data acquisition is limited to the time of the delay of the BOLD contrast after an EEG event (3 sec), although data of the BOLD contrast would be available for 10 sec. But only with this limitation is it possible to exclude the influence of unwanted EEG-events on the image contrast by evaluation of the 3 sec of EEG between the event and the scan. Highly resolved or repeated scans with several slices easily exceed this time limitation, even with the fastest imaging techniques (such as echo-planar imaging (EPI)). To enhance the functional image contrast, images from a state without brain activation (baseline) are statistically correlated with images from an activated state after the desired event (13,14), such as an epileptic discharge in an EEG. To acquire baseline images without unwanted EEG events the image time is limited to 3 sec, with a break of at least 3 sec between the acquisitions. This doubles the scan time, but is essential for the quality of a functional study. It was the aim of our study to understand the generation of artifacts in the EEG and to provide a method to detect epileptic discharges (spikes) in the EEG recorded during MR data acquisition. This would allow the use of longer scans with higher resolutions during the time when the BOLD contrast is enhanced after a single event in the EEG. We have previously demonstrated that EEGs recorded during a fast low angle shot (FLASH) sequence with a short repetition time (TR) can be restored by low-pass filtering, if the frequency window of the EEG ( Hz) is not affected with interference by the scan (6). But this was not the case with the EPI techniques that are widely used for fmri. MATERIALS AND METHODS All measurements were performed on a 1.5 T Magnetom Vision whole body scanner (Siemens, Erlangen, Germany), equipped with an EPI booster at a rise time of 300 sec. A circular, polarized head coil was used. Restoration of an EEG recorded in an MR environment requires an EEG amplifier that is not saturated by any activity of the scanner. That means that to digitally process the EEG, the amplitudes of the artifacts in the EEG during a scan must be in the dynamic range of the amplifier. The EEG amplifier (EMR; Schwarzer GmbH, Munich, Germany) was specifically designed for operation in an MR system and was developed in cooperation with our institute. This device is battery-powered and contains no ferrous material. In one unit the data of 32 channels are amplified, low-pass filtered to avoid aliasing ( 3 db at 450 Hz), and sampled at a rate of 1 khz with a resolution of 65 nv/bit and a dynamic range of 2 mv. The digital information is transferred out of the shielded MR cabin by fiber optics to a PC. The dimensions of the amplifier (13 cm 16 cm 7.5 cm), the electrodes (6 mm diameter), and cables (0.8 mm diameter) were minimized to reduce

2 792 Hoffmann et al. FIG. 1. Power spectral density of 1 sec of an EEG recorded during repeated saturation RF pulses at 64 MHz within SAR limitations. Main frequencies of the RF can be detected at 175 Hz and 350 Hz with a bandwidth of about 50 Hz. the area for eddy currents on leading surfaces near the head to guarantee adequate image quality. The amplifier was located about 0.5 m behind the head coil. The safety of the volunteers and patients was our primary concern. Exposure of the subjects to currents and RF energy coupling into the conducting loop formed by the head, the electrode wires, and the EEG device was eliminated by the high input impedance of the amplifier ( 10 8 ) and by the additional hardware low-pass filter at every input (DC resistance of 64 k and attenuation of 180 db at 64 MHz) (15). Shielded electrode wires were used to avoid conducting loops by capacitive connections of crossing wires (type CX9711, 50, outer diameter 0.8 mm). The material of the electrodes was sintered Ag-AgCl. The high specific resistance of this amorphous material prevented eddy currents and the heating by RF (15,16). EEGs of five healthy volunteers (four males, one female, years old) and five epileptic patients (two males, three females, years old) were recorded in the MR scanner. The approval of the local ethics committee, according to the international convention of Helsinki, was obtained for all EEG recordings during MRI. All subjects gave their informed, written consent for the study. Twenty-one electrodes were placed on the scalp according to the standard electrode positions with an electrode cap. Electrode-skin impedance was under 5 k. The EEG was displayed in the recording software BrainLab (OSG, Rumst, Belgium) using a referential montage to a common reference of several electrodes ( Goldman ) or to a reference of one electrode (Cz), or using a bipolar longitudinal montage. Three channels of ECG were recorded synchronously. To control the quality of the EEG, typical EEG patterns were provoked by commands to the subjects to open and close their eyes. To reduce artifacts in the EEG by any movements of the electrode cables in the high magnetic field, the head of the subject was fixed in the head coil. Electrode wires were fixed on the electrode cap and bound together from the top FIG. 2. Power spectral density of 10 sec of an EEG recorded during a FLASH sequence with a TR of 30 msec. The corresponding interfering frequencies at multiples of 33.3 Hz are high, sharp peaks. The minor contributions of the EEG at frequencies between 0 and 30 Hz can be seen also. of the head to the amplifier. The area of a loop via head, electrodes, and amplifier was thus minimized and ECGsynchronous artifacts were reduced. If ECG-synchronous artifacts were still unacceptably high they were removed by ECG-triggered subtraction of an averaged artifact, as already proposed by our group (6) and by Allen (7). Padding under the electrode wires and the amplifier reduced the mechanical transmission of the vibrations of the MRI scanner during imaging to the EEG system. Coaxial electrode cables with the shield connected to the amplifier were used to reduce all capacitive coupling disturbances. In addition, coaxial electrode cables with shields connected on the one end to the amplifier and on the other end to the shield of a neighboring electrode were tested to reduce inductive coupling disturbances. With the five healthy subjects, we investigated the influence of MR sequence parameters on the interfering frequencies. We programmed testing sequences to apply sin- FIG. 3. The loop structure of the used EPI sequence and the TRs of the single loops: 3.36 msec for phase coding, 135 msec for imaging of one slice, 1628 msec for one whole measurement.

3 EEG During EPI 793 Amplitude of Interference FIG. 4. Power-spectral density of the interference of the EPI sequence depicted in Fig. 2 during an EEG recording. Multiples of 0.61 Hz and 7.36 Hz are clearly detectable, corresponding to the TRs of 1628 msec and 135 msec in the loop structure of the sequence. Amplitudes of the interference are five orders of magnitude higher than in the RF itself. gle components of a sequence, such as repeated RF pulses and oscillating gradients, separately. Standard MR sequences, such as spin echo and gradient echo sequences with different TE and TR values, were performed during EEG recording. The influence of an EPI sequence on EEG recordings was examined since this sequence has successfully been used for functional studies in our institute. The EPI sequence had a TR of 1.68 msec, an echo time of 64 msec, and a flip angle of 90, imaging a matrix at a 6/8 FOV of 280 mm. Fat-saturation was implemented. Ten slices 5 mm thick were measured and the measurements were repeated 10 times without delay. The frequencies induced in an EEG by the EPI sequence were analyzed and compared with the timing of the sequence. The EEGs of five patients with focal epilepsy was recorded during the described EPI sequence. All patients previously underwent long-term video and surface EEG recordings, and only patients with more than 200 interictal spikes per hour were selected for this study. These patients were on anti-epileptic medication and were seizurefree for the last three months. The EEGs were exported and digitally processed with the mathematical tool MATLAB (Math Works, Inc., Natick, MA) and with the EEG processing tool FEMR (Schwarzer GmbH, Munich, Germany), which could also perform subtraction of ECG-related artifacts. RESULTS No subject reported any discomfort during the examinations. Artifact-free imaging was possible in all applications of the EEG setup described above. The EEG amplifier was never saturated by any activity from the MRI scanner, and this allowed digital processing of the interfered EEG. The time derivative of the magnetic flux of the gradients is proportional to the voltage induced in the EEG. The amplitude of interference of an MR sequence was dependent on all sequence parameters regarding the gradient slope (amplitude at a fixed rise time). Therefore, reduction of the slice thickness or the FOV resulted in a higher amplitude of interference. Fixation of the head and the electrode wires on the head influenced the amplitudes as well. The better the wires were fixed on the head and bound together to the amplifier, the lower the amplitude of the ECG-synchronous pulse artifact and of the interference due to scanner activity, because the area of the inductive loop formed by the electrodes, the head, and the amplifier was minimized. Padding under the electrode wires and the amplifier additionally reduced the amplitude of EEG artifacts during the scan. The mechanical forces on the gradient coils when their fields are switched in the static magnetic field induce vibrations in the MRI scanner which are heard as the typical noise. These vibrations transmit to the amplifier and the electrode cables and if they are moved in the high static magnetic field, a disturbing signal is induced according to Faraday s induction law. Different montages of the EEG channels (bipolar or common reference amplification) transferred the maximum amplitudes of interference to different EEG channels. The lowest interference within all channels was observed with a common reference out of 19 channels ( Goldman 19 ). With the optimized EEG setup a switched gradient of one axis with an amplitude of 25 mt/m and a rise time of 300 sec induced a maximum signal of 600 V in the EEG. The three different gradient axes produced different distributions of the interference over the channels, but the maximum amplitudes were in the same range. The interference generated by the RF alone in repeated saturation pulses had a maximum amplitude of 50 V. We did not observe a reduction of the amplitudes of interference using electrodes with both ends of the shield connected to the amplifier compared to the standard shield. Interfering Frequencies If a signal of any shape and any own frequency is continuously repeated after a time t R, the frequency spectrum of a long period of repetitions of that signal consists of multiples of one frequency, that is 1/t R (17). MR sequences consist of several repeated loops of RF and gradient switching. In all the spectra of the EEG with the interference of the applied imaging sequences, multiple discrete frequencies were observed corresponding to TRs of the loops of the MR sequence (harmonics). The own frequencies of the oscillation of the gradients (833 Hz corresponding to 300 sec rise time) or the RF itself (64 MHz) were not observed, because these frequencies were higher than half the sampling rate of the amplifier and were eliminated by the low-pass filter to avoid aliasing. The power spectrum of the repeated saturating RF pulses mainly showed contributions at 175 Hz and at the next multiple of 350 Hz, with a bandwidth of about 50 Hz and power less than 5 V 2 /Hz (Fig. 1). The 175 Hz level

4 FIG. 5. a: Eighteen-channel EEG recording of an epilepsy patient with over 20 spikes per min from different brain areas recorded during the EPI sequence: five measurements with 10 slices each. b: Same EEG filtered by a high-pass filter (0.5 Hz), a low-pass filter (40 Hz) and band-stop filters corresponding to the frequencies by loop structures in the EPI sequence. Several right occipital spikes are clearly detectable.

5 EEG During EPI 795 corresponded to the repetition rate of the saturation pulses we used in this sequence without gradient switching (5710 sec). The frequency spectrum of the gradients alone consisted of multiples of one frequency that corresponded to the repetition rate of an ensemble of gradients. The interfering frequencies of the spin echo and the FLASH sequence consisted of multiples of one frequency that were defined by TR. Figure 2 shows the power spectrum of a T 1 - weighted FLASH with a TR of 30 msec. Besides the multiples of the corresponding frequency of 33.3 Hz with powers over 10 4 V 2 /Hz, the contribution of the EEG can be seen at frequencies between 0 and 25 Hz. For the EPI sequence, the spectrum of interfering frequencies was more complex, but it can be explained by examining the loop structure of this sequence (Fig. 3). The most inner loop represents the readout of the lines. The TR for this loop is twice TR. In our sequence the TR was 1.68 msec, so the frequencies generated by this loop were multiples of 298 Hz. The next outer loop represents the number of acquisitions. Since this number was one in our sequence, it produced no new frequencies. The next outer loop represents the different slices. We imaged 10 slices, and the TR for this loop consisted of the fat saturation, the excitation of the slice, the loop for the lines that is repeated with half the number of lines (64 lines), and timing elements for TR and TD. For the loop of the slices, this resulted in a TR of 136 msec. The corresponding frequencies were multiples of 7.36 Hz and affected the EEG. The most outer loop represents the number of measurements performed. In our study we imaged 10 slices and the time for one complete measurement was 1628 msec. The corresponding frequency was 0.61 Hz. All of these frequencies were found in a power spectrum of an EEG recorded during the sequence (Fig. 4). The powers of the interfering frequencies of the EPI sequence were typically over 10 5 V 2 /Hz. The main contribution to the spectrum was made by the loop for the slices with multiples of 7.36 Hz. The repetition of the measurement produced neighboring frequencies with a distance of 0.61 Hz. Algorithms to Restore the EEG All disturbing frequencies outside the frequency window of the EEG ( Hz) could be eliminated by high- or FIG. 6. Maximum Fourier spectrum smoothed by a Savitzky-Golay filter out of 10 sections of one EEG channel with a duration of 10 sec each, recorded inside the magnet during off scanning. low-pass filters without damage to the EEG, but within this range all frequencies generated by MRI must be selectively removed. In contrast to the discrete peaks contributed by the MRI scanner in the frequency spectrum of an affected EEG, epileptic spikes have a continuous flat spectrum. A spike is a sharp ( 100 msec), high peak in the EEG; it can be compared with a Dirac pulse, whose fast Fourier transform (FFT) consists of constant contributions of all frequencies. When single discrete frequencies are removed from the FFT of an EEG, no essential information concerning the spikes is lost. If the interfering frequencies are known from the loop structure of the sequence or from an FFT of the sequence, a series of band-stop filters can be used to eliminate the interference. To restore the EEG during the EPI sequence, we applied band-stop filters with 3 db frequencies at multiples of 7.36 Hz and at neighboring frequencies 0.61 Hz apart in the frequency window of the EEG. The digital filters were of the fourth order, had a Butterworth characteristic, and a bandwidth of 0.2 Hz. Figure 5a shows all channels of the disturbed EEG during EPI of a patient with FIG. 7. a: The channel O2-Cz of Fig. 5 restored by FFT processing. b: The same channel restored by band-stop filtering. Spikes appear even higher and sharper in a than in b.

6 FIG. 8. a: Twenty channels of EEG of a epileptic patient with 80 spikes per hr in the left temporo-parietal brain area recorded during EPI. b: A minor spike becomes detectable in the FFT-processed EEG.

7 EEG During EPI 797 FIG. 9. a: One channel of an unaffected EEG recorded during off scanning. b: The same unaffected EEG channel after undergoing the same FFT processing as the EEG of Fig. 7a. The differences between a and b are hard to detect, although over 40% of the frequencies in the frequency window of the EEG were discarded. over 20 spikes per min from different brain areas. Fig. 5b is the filtered version, in which various epileptic spikes become clearly detectable in all channels. The restored EEG is consistent with the EEG of the patient recorded under normal conditions. Contributions of the MRI scanner in the frequency spectrum of an affected EEG can also be detected automatically by their high amplitude at discrete frequencies. To find the frequencies contributed by the MRI scanner we used an algorithm that compares the frequency power spectrum of the unaffected EEG with the spectrum of a disturbed EEG of the same channel. We calculated the spectra of 10 different 10-sec-long sections of the unaffected EEG. All sections were from the same channel and were distributed over the entire EEG recording time (about 45 min). The frequency resolution of the spectra was 0.1 Hz. All 10 spectra of the sections were combined into one spectrum, which consisted of the maximum contribution of the 10 EEG sections at every frequency. We then used a Savitzky- Golay smoothing filter to smooth the maximum spectrum (18). With this algorithm, at every data point of the spectrum a polynomial of the degree m is fitted to the n before and after the data points. The value of the polynomial at the data point in the middle is the smoothed value. The degree m of the polynomial was set to 3 and the number of neighboring data points was 16. The smoothed spectrum can be regarded as an envelope of the unaffected EEG spectra of this EEG channel and is shown in Fig. 6. If the value of a frequency in the spectrum of the disturbed EEG was more than 50% higher than the value of the envelope of unaffected EEGs at this frequency, the complex value at this frequency in the FFT of the affected EEG was set to zero. This avoided a changed appearance of the EEG by incorrect phases in reduced frequency values. Thus, the restored EEG only contained less but original frequencies with correct phases. At other times of the recording no FFT of a section of unaffected EEG could be found that exceeded the threshold defined by 150% of the smoothed maximum spectrum. Finally the corrected FFT of the affected EEG was retransformed. The advantages of this processing compared to filtering in the time domain are shown with the EEG channel O2-Cz in Fig. 5. Spikes appear higher and sharper for the FFT processing (Fig. 7a) than when filtering was done in the time domain (Fig. 7b). Figure 8a depicts the EEG of another patient during EPI. Figure 8b shows the same recording after the FFT processing. Even a minor spike with an amplitude of only 70 V can be detected. The spike is sharp (duration 100 msec) and is followed by a slow wave complex. It appears in the left temporo-parietal brain area, where it also was detected in the long-term EEG session. The same frequencies that were removed from the disturbed EEG were also removed from the FFT of an unaffected EEG to control the quality of the EEG in this process (Fig. 9). The differences before (Fig. 9a) and after (Fig. 9b) the process are hard to detect, although over 40% of the frequencies in the frequency window of the EEG were discarded. This validated that the processing does not affect the EEG quality. The presented processes of EEG allowed reliable spike detection during EPI data acquisition with four of the five patients. One patient obviously had no spikes during EPI. DISCUSSION The goal of combining EEG and MRI is the noninvasive detection of epileptic foci by a spike-triggered fmri with EPI techniques. In this study we demonstrated the feasibility of detecting epileptic discharges in the EEG recorded during an EPI sequence. The prerequisite for an EEG eventrelated fmri study is a sufficient number of events during the examination period, but the higher the number of events, the higher the chance for unwanted events during the scan. With the methods presented here, it is possible to ensure the quality of a highly resolved fmri study, with scan times longer than three seconds, by analysis of brain activity during the scan. These methods are not recommended to restore EEG signals of discrete frequencies (such as alpha waves) during an EPI sequence. One of the multiples of the interfering frequencies during imaging might coincidence with the frequency of alpha activity (10 13 Hz) in the EEG and the elimination of interfering frequencies may result in a reduction of the alpha activity. In general, there are two ways to apply the process of EEG recorded in MRI: 1) make the signal instantly visible

8 798 Hoffmann et al. on the EEG recording during an MRI sequence, and 2) accurately restore a recorded signal. With on-line recording, a short calculation time is preferred over accuracy of the processing. The frequency resolution of an FFT or band-stop filter is proportional to the time of the processed signal. For a real-time processing of the EEG there is always the delay of the required time for frequency resolution. Recently, a method was presented to reduce the scanner artifacts in EEG of rats in a7tsystem (19). An interface between the MR scanner and the EEG recording station was used to continuously determine and eliminate the interfering frequencies of the MR scanner within time sections of 300 msec. Therefore, the achieved frequency resolution for restoring the EEG was 3.3 Hz. With time sections of 10 sec, as shown in our study, the EEG is restored with a frequency resolution of 0.1 Hz. While interfering frequencies of the MR imager are very discrete (bandwidth 0.5 Hz), a high frequency resolution of the restoration avoids an affect on the EEG by the processing. But a real-time application is only possible at low frequency resolutions. Other methods to restore electrophysiological signals recorded during MRI have been proposed. However, these were used to restore signals of much higher amplitudes and were therefore of much higher signal-to-noise ratios, such as ECG (20). Our study presents the first human EEG recordings acquired during EPI. The results are encouraging and strongly suggest that a combination of EEG and fmri is a promising and applicable tool for studying functional changes in the human brain. ACKNOWLEDGMENTS The results presented here are part of the doctoral thesis of A. Hoffmann at the Institute for Diagnostic Radiology, Klinikum Grosshadern, University of Munich. REFERENCES 1. Warach S, Ives JR, Schlaug G, Patel MR, Darby DG, Thangaraj V, Edelman RR, Schomer DL. EEG-triggered echo-planar functional MRI in epilepsy. Neurology 1996;47: Ives JR, Warach S, Patel MR, Schlaug G, Edelman RR, Schomer DL. Techniques for monitoring the EEG and triggering functional magnetic resonance imaging scans time-locked to the patient s focal or generalized epileptic discharges. Epilepsia 1995;36:S Krakow K, Woerman FG, Symms MR, Allen PJ, Lemieux L, Barker GJ, Duncan JS, Fish DR. EEG-triggered functional MRI of interictal epileptiform activity in patients with partial seizures. Brain 1999;122: Ives JR, Warach S, Schmitt F, Edelman RR, Schomer DL. Monitoring the patient s EEG during echo planar MRI. Electroencephalogr Clin Neurophysiol 1993;87: Huang-Hellinger FR, Breiter CH, McCormack G, Cohen MS, Kwong KK, Sutton JP, Savoy RL, Weisskopf RM, Davis TL, Baker JR, Belliveau JW, Rosen BR. Simultaneous functional magnetic resonance imaging and electrophysiological recording. Hum Brain Map 1995;3: Jäger L, Hoffmann A, Joppich M, Reiser M. Simultaneous EEG recording with MR data-acquisition. In: Proceedings of the 6th Annual Meeting of ISMRM, Sydney, p Allen PJ, Polizzi G, Krakow K, Fish DR, Lemieaux L. Identification of EEG events in the MR scanner: the problem of pulse artifact and a method for its subtraction. Neuroimage 1999;8: Hill RA, Chiappa KH, Huang-Hellinger F, Jerkins BG. EEG during MR imaging: differentiation of movement artifact from paroxysmal cortical activity. Neurology 1995;45: Müri RM, Felbinger J, Rösler KM, Jung, Hess CW, Boesch C. Recording of electrical brain activity in a magnetic resonance environment: distorting effects of the static magnetic field. Magn Reson Med 1998;39: Ogawa S, Lee TM, Kay AR, Tank DW. Brain magnetic resonance imaging with contrast dependent on blood oxygenation. Proc Natl Acad Sci USA 1990;89: Buckner RL, Goodman J, Burock M, Rotte M, Koutstaal W, Schacter D, Rosen B, Dale AM. Functional-anatomic correlates of object priming in humans revealed by rapid presentation event-related fmri. Neuron 1998;20: Rosen BR, Buckner RL, Dale AM. Event-related functional MRI: Past, present, and future. Proc Natl Acad Sci USA 1998;95: Bandettini PA, Jesmanowicz A, Wong EC, Hyde JS. Processing strategies for time-course data sets in functional MRI of the human brain. Magn Reson Med 1993;30: Cox RW, Jesmanowicz A, Hyde JS. Real-time functional magnetic resonance imaging. Magn Reson Med 1995;33: Lemieux L, Allen PhJ, Franconi F, Symms MR, Fish DR. Recording of EEG during fmri experiments: patient safety. Magn Reson Med 1997; 38: von Smekal A, Seelos KC, Kuper CR, Reiser M. Patient monitoring and safety during MRI examinations. Eur Radiol 1995;5: Bracewell RN. The Fourier transform and its applications. Singapore: McGraw-Hill Book Co; p. 18. Press WA, Teukolsky SA, Vetterling WT, Flannery BP. Numerical recipes in C. Cambridge: University Press; p. 19. Sijbers J, Michiels I, Verhoye M, van Audekerke J, van der Linden A, van Dyck D. Restoration of MR-induced artifacts in simultaneously recorded MR/EEG data. Magn Reson Imaging 1999;17(9): Felblinger J, Slotboom J, Kreis R, Jung B, Boesch C. Restoration of electrophysiological signals distorted by inductive effects of magnetic field gradients during MR sequences. Magn Reson Med 1999;41(4):