Camera-based Prospective Motion Correction in Paediatric Epilepsy Patients Enables EEG-fMRI Localization Even in High-motion States

Abstract

Background: EEG-fMRI is a useful additional test to localize the epileptogenic zone (EZ) particularly in MRI negative cases. However subject motion presents a particular challenge owing to its large effects on both MRI and EEG signal. Traditionally it is assumed that prospective motion correction (PMC) of fMRI precludes EEG artifact correction.

Methods: Children undergoing presurgical assessment at Great Ormond Street Hospital were included into the study. PMC of fMRI was done using a commercial system with a Moiré Phase Tracking marker and MR-compatible camera. For retrospective EEG correction both a standard and a motion educated EEG artefact correction (REEGMAS) were compared to each other.

Results: Ten children underwent simultaneous EEG-fMRI. Overall head movement was high (mean RMS velocity < 1.5 mm/s) and showed high inter- and intra-individual variability. Comparing motion measured by the PMC camera and the (uncorrected residual) motion detected by realignment of fMRI images, there was a five-fold reduction in motion from its prospective correction. Retrospective EEG correction using both standard approaches and REEGMAS allowed the visualization and identification of physiological noise and epileptiform discharges. Seven of 10 children had significant maps, which were concordant with the clinical EZ hypothesis in 6 of these 7.

Conclusion: To our knowledge this is the first application of camera-based PMC for MRI in a pediatric clinical setting. Despite large amount of movement PMC in combination with retrospective EEG correction recovered data and obtained clinically meaningful results during high levels of subject motion. Practical limitations may currently limit the widespread use of this technology.

Keywords: Drug-resistant epilepsy; EEG-fMRI; Pediatric epilepsy; Prospective motion correction.

Fig. 1

Example of EEG correction from (patient 2, run 2; Brain Vision Analyzer 2 and REEGMAS), 50 s duration, during a period of low motion as indicated by PMC (± 2.5 mm) and RP data (± 0.5 mm)

Fig. 2

Example of EEG correction (patient 2, run 2; Brain Vision Analyzer 2 and REEGMAS), 50s duration, during a period of high motion as indicated by PMC (± 7 mm) and RP data (± 1.4 mm)

Fig. 3

Motion traces of fMRI run 2 of patient 4; upper panel shows head motion in the scanner over time as detected by the PMC camera; lower panel shows SPM realignment parameters over time corresponding to the PMC data. Example of EEG correction (Brain Vision Analyzer 2 and REEGMAS), 50s duration, during a period of high motion as indicated by PMC (± 10 mm) and RP data (± 1 mm)

Fig. 4

Averaged variances of raw EEG data and EEG data post correction using the different correction methods for data acquired simultaneously to prospective motion corrected fMRI. For each patient and fMRI run the variance was calculated for each slice TR and from these the average variance was calculated for the raw EEG (blue), EEG corrected for GA using standard AAS (red) and REEGMAS (yellow) considering all electrodes but excluding ECG. The standard error on the mean variance is presented by the error bars. The blue * highlights templates with averaged variance significantly smaller than the variance of the Raw EEG and the red * highlight runs where the average variance for the data corrected by REEGMAS are significantly smaller than the variance of the data resulting from standard AAS GA correction

Fig. 5

The mean power spectral density (PSD) at electrode Fp1 for each patient. The mean PSD for each patient is presented for the EEG run with the highest averaged variance for the Raw EEG data (Fig. 5). The shaded grey area represents two standard deviations from the mean baseline spectra obtained from EEG data from outside the MRI scanner. The blue curve refers to the mean power spectra of the EEG acquired in-scanner but not corrected by REEGMAS and the red dashed line to the same data corrected by REEGMAS. Electrode Fp1 is shown due to its clinical relevance for this patient population

Fig. 6

PMC velocity in mm per second and Euclidian displacement as detected by the PMC-camera system and realignment parameters (RP) of the first fMRI run of patient 5. At approx. 480 s a very large peak can be seen. Occurring mostly in the z-axis

Fig. 7

Linear Regression of median root mean square (RMS) of realignment parameters (RP) and RMS of Euclidian displacement of measured motion from the prospective motion correction (PMC); 95% CI: 95% confidence interval

Fig. 8

Linear Regression of FIACH tSNR and median RMS of Euclidian displacement of prospective motion correction (PMC); 95% CI: 95% confidence interval

Fig. 9

Median RMS of Euclidian displacement of prospective motion correction (PMC) over FIACH voxels replaced; y = slope x intercept; 95% CI: 95% confidence interval

Fig. 10

fMRI (upper panel) and ESI results (second panel) of patient 4 showing a concordant left frontal focus; the cross-hair/ cross marks the point of maximal activation/ electrical activity. The lower two panels show the amount of movement in the concordant fMRI run as recorded by the camera before (PMC) and after (RP) prospective motion correction