Exploring the feasibility of simultaneous electroencephalography/functional magnetic resonance imaging at 7 T

The increased blood oxygenation level-dependent contrast available at high field makes the implementation of combined EEG/fMRI experiments at 7 T highly worthwhile from the point of view of fMRI data quality, but the higher field poses greater technical challenges for achieving good quality EEG data. A study of the feasibility of recording EEG signals from human subjects at 7 T using a commercially available, MR-compatible EEG system has therefore been carried out. This involved systematic measurement of the sources of noise in EEG recordings made in the 7 T scanner and measurement of RF heating effects on a gel phantom in the presence of a 32-electrode EEG cap. Having found no significant safety concerns and identified a set-up (involving switching off the magnet's cryo-cooler pumps and mounting the EEG amplifier on a cantilever) that limited scanner-induced noise, combined EEG/fMRI experiments employing visual stimulation were then successfully carried out on two human subjects. With the use of beamformer-based analysis of the EEG data, driven responses and alpha-band, event-related desynchronisation were identified in both subjects.     

Continuous EEG-fMRI in patients with partial epilepsy and focal interictal slow-wave discharges on EEG

Purpose

To verify whether in patients with partial epilepsy and routine electroenecephalogram (EEG) showing focal interictal slow-wave discharges without spikes combined EEG–functional magnetic resonance imaging (fMRI) would localize the corresponding epileptogenic focus, thus providing reliable information on the epileptic source.

Methods

Eight patients with partial epileptic seizures whose routine scalp EEG recordings on presentation showed focal interictal slow-wave activity underwent EEG–fMRI. EEG data were continuously recorded for 24 min (four concatenated sessions) from 18 scalp electrodes, while fMRI scans were simultaneously acquired with a 1.5-Tesla magnetic resonance imaging (MRI) scanner. After recording sessions and MRI artefact removal, EEG data were analyzed offline. We compared blood oxygen level-dependent (BOLD) signal changes on fMRI with EEG recordings obtained at rest and during activation (with and without focal interictal slow-wave discharges).

Results

In all patients, when the EEG tracing showed the onset of focal slow-wave discharges on a few lateralized electrodes, BOLD-fMRI activation in the corresponding brain area significantly increased. We detected significant concordance between focal EEG interictal slow-wave discharges and focal BOLD activation on fMRI. In patients with lesional epilepsy, the epileptogenic area corresponded to the sites of increased focal BOLD signal.

Conclusions

Even in patients with partial epilepsy whose standard EEGs show focal interictal slow-wave discharges without spikes, EEG–fMRI can visualize related focal BOLD activation thus providing useful information for pre-surgical planning.     

EEG quality during simultaneous functional MRI of interictal epileptiform discharges

This article concerns the evaluation of the quality of interictal epileptiform EEG discharges recorded throughout simultaneous echo planar imaging (EPI). BOLD (blood oxygen level dependent) functional MRI (fMRI) images were acquired continuously on a patient with intractable epilepsy. EEG was sampled simultaneously, during and after imaging, with removal of pulse and imaging artifacts by subtraction of channel-specific running averages. Contiguous EEG epochs recorded with and without fMRI (fMRI+ve vs. fMRI−ve) were next randomized and presented to two blinded observers. Epileptiform discharges were identified retrospectively, and comparison was made in terms of the number of identified events, their amplitude, and spatiotemporal distribution. A spectral analysis was also performed on the EEG. In the randomized comparison of EEG segments, 80 (fMRI+ve) vs. 69 (fMRI−ve) discharges were noted with good interobserver agreement (69%). There were no significant differences in amplitude or spatio-temporal distribution. Comparison of the events detected and measured by two expert observers demonstrated that the Interictal Epileptiform Discharge (IED) characteristics were indistinguishable with and without scanning. We review briefly the existing literature on EEG recording quality for combined EEG/fMRI.     

Real-time MR artifacts filtering during continuous EEG/fMRI acquisition

The purpose of this study was the development of a real-time filtering procedure of MRI artifacts in order to monitor the EEG activity during continuous EEG/fMRI acquisition. The development of a combined EEG and fMRI technique has increased in the past few years. Preliminary “spike-triggered” applications have been possible because in this method, EEG knowledge was only necessary to identify a trigger signal to start a delayed fMRI acquisition. In this way, the two methods were used together but in an interleaved manner. In real simultaneous applications, like event-related fMRI study, artifacts induced by MRI events on EEG traces represent a substantial obstacle for a right analysis. Up until now, the methods proposed to solve this problem are mainly based on procedures to remove post-processing artifacts without the possibility to control electrophysiological behavior of the patient during fMRI scan. Moreover, these methods are not characterized by a strong “prior knowledge” of the artifact, which is an imperative condition to avoid any loss of information on the physiological signals recovered after filtering. In this work, we present a new method to perform simultaneous EEG/fMRI study with real-time artifacts filtering characterized by a procedure based on a preliminary analytical study of EPI sequence parameters-related EEG-artifact shapes. Standard EEG equipment was modified in order to work properly during ultra-fast MRI acquisitions. Changes included: high-performance acquisition device; electrodes/cap/wires/cables materials and geometric design; shielding box for EEG signal receiver; optical fiber link; and software. The effects of the RF pulse and time-varying magnetic fields were minimized by using a correct head cap wires-locked environment montage and then removed during EEG/fMRI acquisition with a subtraction algorithm that takes in account the most significant EPI sequence parameters. The on-line method also allows a further post-processing utilization.     

EEG-fMRI mapping of asymmetrical delta activity in a patient with refractory epilepsy is concordant with the epileptogenic region determined by intracranial EEG

We studied a patient with refractory focal epilepsy using continuous EEG-correlated fMRI. Seizures were characterized by head turning to the left and clonic jerking of the left arm, suggesting a right frontal epileptogenic region. Interictal EEG showed occasional runs of independent nonlateralized slow activity in the delta band with right frontocentral dominance and had no lateralizing value. Ictal scalp EEG had no lateralizing value. Ictal scalp EEG suggested right-sided central slow activity preceding some seizures. Structural 3-T MRI showed no abnormality. There was no clear epileptiform abnormality during simultaneous EEG-fMRI. We therefore modeled asymmetrical EEG delta activity at 1-3 Hz near frontocentral electrode positions. Significant blood oxygen level-dependent (BOLD) signal changes in the right superior frontal gyrus correlated with right frontal oscillations at 1-3 Hz but not at 4-7 Hz and with neither of the two frequency bands when derived from contralateral or posterior electrode positions, which served as controls. Motor fMRI activations with a finger-tapping paradigm were asymmetrical: they were more anterior for the left hand compared with the right and were near the aforementioned EEG-correlated signal changes. A right frontocentral perirolandic seizure onset was identified with a subdural grid recording, and electric stimulation of the adjacent contact produced motor responses in the left arm and after discharges. The fMRI localization of the left hand motor and the detected BOLD activation associated with modeled slow activity suggest a role for localization of the epileptogenic region with EEG-fMRI even in the absence of clear interictal discharges.     

Synchronized and noise-robust audio recordings during realtime magnetic resonance imaging scans

This letter describes a data acquisition setup for recording, and processing, running speech from a person in a magnetic resonance imaging (MRI) scanner. The main focus is on ensuring synchronicity between image and audio acquisition, and in obtaining good signal to noise ratio to facilitate further speech analysis and modeling. A field-programmable gate array based hardware design for synchronizing the scanner image acquisition to other external data such as audio is described. The audio setup itself features two fiber optical microphones and a noise-canceling filter. Two noise cancellation methods are described including a novel approach using a pulse sequence specific model of the gradient noise of the MRI scanner. The setup is useful for scientific speech production studies. Sample results of speech and singing data acquired and processed using the proposed method are given.     

Special designed RF-antenna with integrated non-invasive carbon electrodes for simultaneous magnetic resonance imaging and electroencephalography acquisition at 7T

The construction of a high quality MR RF-antenna with incorporated EEG electrodes for simultaneous MRI and EEG acquisition is presented. The antenna comprises an active decoupled surface coil for receiving the MR signal and a whole body coil for transmitting the excitation RF pulses. The surface coil offers a high signal-to-noise ratio required for fMRI application and the whole body coil has a good B(1) excitation profile, which enables the application of homogeneous RF pulses. Non-invasive carbon electrodes are used in order to minimise the magnetic susceptibility artefacts that occur upon application of conductive materials. This dedicated set-up is compared to a standard set-up being a linear birdcage coil and commercially available Ag/AgCl electrodes. As the acquired EEG signals are heavily disturbed by the gradient switching, intelligent filtering is applied to obtain a clean EEG signal.     

A novel functional magnetic resonance imaging compatible search-coil eye-tracking system

Measuring eye movements (EMs) using the search-coil eye-tracking technique is superior to video-based infrared methods [Collewijn H, van der Mark F, Jansen TC. Precise recording of human eye movements. Vision Res 1975;15(3):447-50], which suffer from the instability of pupil size, blinking behavior and lower temporal resolution. However, no conventional functional magnetic resonance imaging (fMRI)-compatible search-coil eye tracker exists. The main problems for such a technique are the interaction between the transmitter coils and the magnetic gradients used for imaging as well as the limited amount of space in a scanner. Here we present an approach to overcome these problems and we demonstrate a method to record EMs in an MRI scanner using a search coil. The system described has a spatial resolution of 0.07 degrees (visual angle) and a high temporal resolution (22 kHz). The transmitter coils are integrated into the visual presentation system and the control/analysis unit is portable, which enables us to integrate the eye tracker with an MRI scanner. Our tests demonstrate low noise in the recorded eye traces and scanning with minimal artifact. Furthermore, the induced current in the search coil caused by the RF pulses does not lead to measurable heating. Altogether, this MR-compatible search-coil eye tracker can be used to precisely monitor EMs with high spatial and temporal resolution during fMRI. It can therefore be of great importance for studies requiring accurate fixation of a target, or measurement and study of the subject's oculomotor system.     

Active control of the volume acquisition noise in functional magnetic resonance imaging: method and psychoacoustical evaluation.

Functional magnetic resonance imaging (fMRI) provides a noninvasive tool for observing correlates of neural activity in the brain while a subject listens to sound. However, intense acoustic noise is generated in the process of capturing MR images. This noise stimulates the auditory nervous system, limiting the dynamic range available for displaying stimulus-driven activity. The noise is potentially damaging to hearing and is distracting for the subject. In an active noise control (ANC) system, a reference sample of a noise is processed to form a sound which adds destructively with the noise at the listener's ear. We describe an implementation of ANC in the electromagnetically hostile and physically compact MRI scanning environment. First, a prototype system was evaluated psychoacoustically in the laboratory, using the electrical drive to a noise-generating loudspeaker as the reference. This system produced 10-20 dB of subjective noise-reduction between 250 Hz and 1 kHz, and smaller amounts at higher frequencies. The system was modified to operate in a real MR scanner where the reference was obtained by recording the acoustic scanner noise. Objective reduction by 30-40 dB of the most intense component in scanner noises was realized between 500 Hz and 3500 Hz, and subjective reduction of 12 dB and 5 dB in tests at frequencies of 600 Hz and at 1.9 kHz, respectively. Although the benefit of ANC is limited by transmission paths to the cochlea other than air-conduction routes from the auditory meatus, ANC achieves worthwhile attenuation even in the frequency range of maximum bone conduction (1.5-2 kHz). ANC should, therefore, be generally useful during auditory fMRI.     

An empirical investigation of motion effects in eMRI of interictal epileptiform spikes

We recently developed a functional neuroimaging technique called encephalographic magnetic resonance imaging (eMRI). Our method acquires rapid single-shot gradient-echo echo-planar MRI (repetition time=47 ms); it attempts to measure an MR signal more directly linked to neuronal electromagnetic activity than existing methods. To increase the likelihood of detecting such an MR signal, we recorded concurrent MRI and scalp electroencephalography (EEG) during fast (20-200 ms), localized, high-amplitude (>50 μV on EEG) cortical discharges in a cohort of focal epilepsy patients. Seen on EEG as interictal spikes, these discharges occur in between seizures and induced easily detectable MR magnitude and phase changes concurrent with the spikes with a lag of milliseconds to tens of milliseconds. Due to the time scale of the responses, localized changes in blood flow or hemoglobin oxygenation are unlikely to cause the MR signal changes that we observed. While the precise underlying mechanisms are unclear, in this study, we empirically investigate one potentially important confounding variable — motion. Head motion in the scanner affects both EEG and MR recording. It can produce brief “spike-like” artifacts on EEG and induce large MR signal changes similar to our interictal spike-related signal changes. In order to explore the possibility that interictal spikes were associated with head motions (although such an association had never been reported), we had previously tracked head position in epilepsy patients during interictal spikes and explicitly demonstrated a lack of associated head motion. However, that study was performed outside the MR scanner, and the root-mean-square error in the head position measurement was 0.7 mm. The large inaccuracy in this measurement therefore did not definitively rule out motion as a possible signal generator. In this study, we instructed healthy subjects to make deliberate brief (<500 ms) head motions inside the MR scanner and imaged these head motions with concurrent EEG and MRI. We compared these artifactual MR and EEG data to genuine interictal spikes. While per-voxel MR and per-electrode EEG time courses for the motion case can mimic the corresponding time courses associated with a genuine interictal spike, head motion can be unambiguously differentiated from interictal spikes via scalp EEG potential maps. Motion induces widespread changes in scalp potential, whereas interictal spikes are localized and have a regional fall-off in amplitude. These findings make bulk head motion an unlikely generator of the large spike-related MR signal changes that we had observed. Further work is required to precisely identify the underlying mechanisms.     

Simultaneous EEG-fMRI acquisition: how far is it from being a standardized technique?

Simultaneous EEG–fMRI is a powerful tool to study spontaneous and evoked brain activity because of the complementary advantages of the two techniques in terms of temporal and spatial resolution. In recent years, a significant number of scientific works have been published on this subject. However, many technical problems related to the intrinsic incompatibility of EEG and MRI methods are still not fully solved. Furthermore, simultaneous acquisition of EEG and event-related fMRI requires precise synchronization of all devices involved in the experimental setup. Thus, timing issue must be carefully considered in order to avoid significant methodological errors.

The aim of the present work is to highlight and discuss some of technical and methodological open issues associated with the combined use of EEG and fMRI. These issues are presented in the context of preliminary data regarding simultaneous acquisition of event-related evoked potentials and BOLD images during a visual odd-ball paradigm.     

Developments in active noise control sound systems for magnetic resonance imaging

Magnetic resonance imaging (MRI) scanners can produce noise measuring over 130 dB SPL. This noise stimulates the auditory nervous system, limiting the dynamic range for stimulus driven activity in functional MRI (fMRI) experiments and can influence other brain functions. Even for structural scans it causes subject anxiety and discomfort in addition to the impediment to communications. Here we describe the realization and validation of a sound system for sound presentation inside an MRI scanner and the modifications to a standard active noise control technique for use in the noisy and compact environment of the scanner. This paper provides a review of the technology available for the presentation of audio stimuli in an MRI environment and the modifications required for the active control of scanner noise. Some of the content has been previously published [Chambers J, Akeroyd MA, Summerfield AQ, Palmer AR. Active control of the volume acquisition noise in functional magnetic resonance imaging: method and psychoacoustical evaluation. J Acoust Soc Am 2001;110(6):3041-54; Levitt H. Transformed up-down methods in psychoacoustics. J Acoust Soc Am 1971;49:467-77], but this paper goes further in describing the stages of development as the system performance was optimised. The performance of the system and both the objective and subjective reduction of the scanner noise are reported. Finally, we discuss recent improvements to the system that are currently being evaluated and describe the theory of opto-acoustical transducers that operate on the principle of light modulation. These are immune from, and do not create, electro-magnetic interference (EMI) and radio-frequency interference (RFI).     

Assessment of data acquisition parameters,and analysis techniques for noise reduction in spinal cord fMRI data

Purpose

The purpose of this work is to characterize the noise in spinal cord functional MRI, assess current methods aimed at reducing noise, and optimize imaging parameters.

Methods

Functional MRI data were acquired at multiple echo times and the contrast-to-noise ratio (CNR) was calculated. Independently, the repetition time was systematically varied with and without parallel imaging, to maximize BOLD sensitivity and minimize type I errors. Noise in the images was characterized by examining the frequency spectrum, and investigating whether autocorrelations exist. The efficacy of several physiological noise reduction methods in both null (no stimuli) and task (thermal pain paradigm) data was also assessed. Finally, our previous normalization methods were extended.

Results

The echo time with the highest functional CNR at 3 Tesla is at roughly 75 msec. Parallel imaging reduced the variance and the presence of autocorrelations, however the BOLD response in task data was more robust in data acquired without parallel imaging. Model-free based approaches further increased the detection of active voxels in the task data. Finally, inter-subject registration was improved.

Conclusions

Results from this study provide a rigorous characterization of the properties of the noise and assessment of data acquisition and analysis methods for spinal cord and brainstem fMRI.     

Activation volume vs BOLD signal change as measures of fMRI activation – Its impact on GABA – fMRI activation correlation

PurposeTo explore the relative robustness of functional MRI (fMRI) activation volume and blood oxygen level-dependent (BOLD) signal change as fMRI metric, and to study the effect of relative robustness on the correlation between fMRI activation and cortical gamma amino butyric acid (GABA) in healthy controls and patients with multiple sclerosis (MS).MethodsfMRI data were acquired from healthy controls and patients with MS, with the subjects peforming self paced bilateral finger tapping in block design. GABA spectroscopy was performed with voxel placed on the area of maximum activation during fMRI. Activation volume and BOLD signal changes at primary motor cortex (M1), as well as GABA concentration were calculated for each patient.ResultsActivation volume correlated with BOLD signal change in healthy controls, but no such correlation was observed in patients with MS. This difference was likely the result of higher intersubject noise variance in the patient population. GABA concentration correlated with M1 activation volume in patients but not in controls, and did not correlate with any fMRI metric in patients or controls.ConclusionOur data suggest that activation volume is a more robust measure than BOLD signal change in a group with high intersubject noise variance as in patients with MS. Additionally, this study demonstrated difference in correlation behavior between GABA concentration and the 2 fMRI metrics in patients with MS, suggesting that GABA - activation volume correlation is more appropriate measure in the patient group.     

Video camera and light system for application in magnetic resonance scanners

The direct observation and simultaneous recording of subject behavior, e.g. facial movements, during MR imaging is necessary for a variety of functional imaging studies involving phenomena such as emotions, humor, mood, etc. Such observation is also valuable for the monitoring of very ill or young patients. We describe a color video camera and light system which works within the functioning scanner. The camera acquires high resolution video sequences during conventional T(1)-weighted and functional T(2)*-weighted imaging. When fixed to the head coil artefacts during the MRI-acquisition were insignificant. The video allows observation of the face detailed enough to permit FACS scoring of facial expressions. We therefore propose that it can be applied for a wide variety of studies needing visual feedback of subject behavior.     

Evaluation of preprocessing steps to compensate for magnetic field distortions due to body movements in BOLD fMRI

Blood oxygenation level-dependent (BOLD) functional magnetic resonance imaging (fMRI) is currently the dominant technique for non-invasive investigation of brain functions. One of the challenges with BOLD fMRI, particularly at high fields, is compensation for the effects of spatiotemporally varying magnetic field inhomogeneities (ΔB₀) caused by normal subject respiration and, in some studies, movement of the subject during the scan to perform tasks related to the functional paradigm. The presence of ΔB₀ during data acquisition distorts reconstructed images and introduces extraneous fluctuations in the fMRI time series that decrease the BOLD contrast-to-noise ratio. Optimization of the fMRI data-processing pipeline to compensate for geometric distortions is of paramount importance to ensure high quality of fMRI data. To investigate ΔB₀ caused by subject movement, echo-planar imaging scans were collected with and without concurrent motion of a phantom arm. The phantom arm was constructed and moved by the experimenter to emulate forearm motions while subjects remained still and observed a visual stimulation paradigm. These data were then subjected to eight different combinations of preprocessing steps. The best preprocessing pipeline included navigator correction, a complex phase regressor and spatial smoothing. The synergy between navigator correction and phase regression reduced geometric distortions better than either step in isolation and preconditioned the data to make them more amenable to the benefits of spatial smoothing. The combination of these steps provided a 10% increase in t-statistics compared to only navigator correction and spatial smoothing and reduced the noise and false activations in regions where no legitimate effects would occur.     

Comparison of analytical strategies for EEG-correlated fMRI data in patients with epilepsy

The simultaneous recording of electroencephalography (EEG) and functional magnetic resonance imaging (fMRI) can be used to localize interictal epileptiform discharges (IEDs). Previous studies have reported varying degrees of concordance of EEG-fMRI with electroclinical findings. The aim of the present study is to evaluate to what extent this variability is determined by the analytical strategy or by the properties of the EEG data. For that purpose, 42 IED sets obtained in 29 patients with epilepsy were reanalyzed using a finite impulse response approach, which estimates the hemodynamic response function (HRF) from the data and allows non-causal effects. Cardiac effects were treated as additional confounders in the model. This approach was compared to the classical approach assuming a fixed HRF for each voxel in the brain. The performance of each method was assessed by comparing the fMRI results to the EEG focus. The flexible model revealed more significantly activated voxels, which resulted in more activated brain regions concordant with the EEG focus (26 vs. 16). Correction for cardiac effects improved the results in 7 out of the 42 data sets. Furthermore, design theory for event-related experiments was applied in order to determine the influence of the number of IEDs and their temporal distribution on the success of an experiment. It appeared that this success is highly dependent upon the number of IEDs present during the recording and less on their temporal spacing. We conclude that the outcome of EEG-fMRI can be improved by using an optimized analytical strategy, but also depends on the number of IEDs occurring during the recording.