Simultaneous intracranial EEG–fMRI in humans: Protocol considerations and data quality

doi:10.1016/j.neuroimage.2012.05.056

NeuroImage

Volume 63, Issue 1, 15 October 2012, Pages 301-309

https://doi.org/10.1016/j.neuroimage.2012.05.056 Get rights and content

Abstract

We have recently performed simultaneous intracranial EEG and fMRI recordings (icEEG–fMRI) in patients with epilepsy. In this technical note, we examine limited thermometric data for potential electrode heating during our protocol and found that heating was ≤ 0.1 °C in-vitro at least 10 fold less than in-vivo limits. We quantify EEG quality, which can be degraded by MRI scanner-induced artefacts, and fMRI image (gradient echo echo-planar imaging: GE-EPI) signal quality around the electrodes, which can be degraded by electrode interactions with B1 (radiofrequency) and B0 (static) magnetic fields. We recorded EEG outside and within the MRI scanner with and without scanning. EEG quality was largely preserved during scanning and in particular heartbeat-related artefacts were small compared to epileptic events. To assess the GE-EPI signal reduction around the electrodes, we compared image signal intensity along paths into the brain normal to its surface originating from the individual platinum–iridium electrode contacts. GE-EPI images were obtained at 1.5 T with an echo time (TE) of 40 ms and repetition time (TR) of 3000 ms and a slice thickness of 2.5 mm. We found that GE-EPI signal intensity reduction was confined to a 10 mm radius and that it was reduced on average by less than 50% at 5 mm from the electrode contacts. The GE-EPI image signal reduction also varied with electrode orientation relative to the MRI scanner axes; in particular, cortical grid contacts with a normal along the scanner's main magnetic field (B₀) axis have higher artefact levels relative to those with a normal perpendicular to the z-axis. This suggests that the artefacts were predominantly susceptibility-related rather than due to B1 interactions. This information can be used to guide interpretation of results of icEEG–fMRI experiments proximal to the electrodes, and to optimise artefact reduction strategies.

Introduction

We have recently reported the first simultaneous intracranial EEG and fMRI (icEEG–fMRI) experiments in humans which were obtained in patients with epilepsy with the aim of mapping and characterising the brain areas associated with epileptic discharges (Vulliemoz et al., 2011). The main technical challenges of recording intracranial EEG (icEEG) and fMRI simultaneously (icEEG–fMRI) are patient safety (Carmichael et al., 2010), MRI scanner-induced EEG artefacts (Allen et al., 1998, Allen et al., 2000) and fMRI image quality degradation (Vulliemoz et al., 2011).

Initial experimental results were encouraging in that the quality of intracranial EEG recorded during fMRI was good based on visual assessment and many more events were detected as compared to scalp EEG–fMRI recordings in the same patients (Vulliemoz et al., 2011), as expected from studies of intracranial and scalp EEG (Tao et al., 2005). However, in order to fully exploit the greater sensitivity of icEEG every effort must be made to capture the electrophysiological activity occurring across a wide frequency range and small spatial scale with minimum contamination from interactions between the EEG and scanning processes. Responses linked to epileptic events were detected within a centimetre of electrode contacts, but there was loss of GE-EPI signal proximal to each electrode contact (Vulliemoz et al., 2011). Visual assessment of the fMRI image data obtained in those studies showed that the extent of the GE-EPI signal loss was dependent on electrode type and location. These observations motivate a more quantitative characterisation of the imaging artefacts.

In this work, we report in-vitro temperature measurements with our study protocol performed prior to patient studies, quantify both the effect of scanning on EEG using spectral analysis and the effect of electrodes on GE-EPI signal intensity in patient data. For the latter, we considered the following factors: electrode type (grid, depth), distance from the electrode, anatomical localisation, and orientation of the electrode relative to the MRI scanner's main magnetic field (B₀, and by convention the z-axis).

Section snippets

In-vitro RF heating safety testing

This set of experiments was designed to complement previously published studies by considering new electrode connection configurations and to determine likely heating effects in the actual configuration used in subsequent patient studies. We previously studied heating in experiments where the electrodes were either all not connected (Carmichael et al., 2008a) or all connected to the EEG recording amplifier (Carmichael et al., 2010). Our MR compatible EEG system can record up to 64 channels but

In vitro temperature measurements

Temperature variations during the entire scanning protocol used for in-vivo experiments (≤ 0.1 W/kg head average SAR) were below the resolution of our temperature measurement system (≤ 0.1 °C). Temperature changes of maximum value 1.5 °C were measured when a high SAR (3.0 W/kg head average) sequence was used. Temperature changes were not increased by partially connecting electrode contacts to the EEG amplifier leaving the remaining electrodes unconnected (but electrically isolated). Temperature data

Discussion

We have quantified EEG and image quality in simultaneously acquired intracranial EEG and fMRI data in humans, to further demonstrate the technique's potential and limitations and set a baseline for possible future developments aimed at improving data quality. We have also described additional temperature measurements we performed to extend our previous studies, and confirm that our patient protocol avoided excessive heating for realistic electrode-lead configurations.

Conclusions

We have performed icEEG–fMRI using a 1.5 T MRI scanner with a head transmit–receive coil, low SAR sequences and electrode leads and wires external to the head with specific lengths and precisely positioned along the RF coil's central z-axis. In this configuration, heating in-vitro was limited to ≤ 0.1 °C, implying a safety factor of 10 in relation to the statutory temperature increase limits. In measurements in two patients icEEG quality during MRI was quantitatively comparable to recordings

Acknowledgments

We are grateful to our colleagues in the Telemetry Unit and the Neuroradiology Department at the National Hospital for Neurology and Neurosurgery (UCLH), Queen Square, London UK for their help in data collection. DC, RR and LL acknowledge the financial support of the UK Medical Research Council (MRC grant G0301067). S. Vulliemoz was supported by a fellowship for advanced researcher and by the SNF grant 33CM30-124089 and 320030‐141165 (SPUM Epilepsy) from the Swiss National Science Foundation.

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Technical NoteSimultaneous intracranial EEG–fMRI in humans: Protocol considerations and data quality

Abstract

Introduction

Section snippets

In-vitro RF heating safety testing

In vitro temperature measurements

Discussion

Conclusions

Acknowledgments

Neuroimage

Neuroimage

J. Magn. Reson. Imaging

Neuroimage

Int. J. Hyperthermia

Epilepsia

Technical Note
Simultaneous intracranial EEG–fMRI in humans: Protocol considerations and data quality