EEG source imaging technique to investigate sleep oscillations for simultaneous EEG-fMRI
Authors: Uji Makoto , Jegou Aude , Cross Nathan E. , Pomares Florence B. , Perrault Aurore A. , Nguyen Alex , Aydin Umit , Lee Kangjoo , Abdallah Chifaou , Frauscher Birgit , Lina Jean-Marc , Dang-Vu Thien Thanh , Grova Christophe 
Published: August 2024

Simultaneous recording of electroencephalography (EEG) and functional magnetic resonance imaging (fMRI) is a widely used non-invasive neuroimaging technique in sleep studies. However, EEG data are strongly influenced by two types of MRI-related artefacts: gradient artefacts (GA) and ballistocardiogram artefacts (BCG). If artefacts correction is suboptimal, the BCG obscures the EEG signals below 20Hz and could make it difficult to investigate sleep oscillations, especially sleep spindles, sleep specific oscillations occurring within 11-16Hz frequency band. We previously demonstrated the utility of beamforming spatial filtering in correcting MRI-related artefacts on EEG. Here, we investigated the use of beamforming spatial filtering for improving the detection of EEG oscillations during sleep, in particular, 1) to accurately estimate single-event spindle EEG power changes, and 2) to demonstrate the potential improvement of fMRI general linear model (GLM) analysis when involving such additional EEG information. We analysed EEG-fMRI data acquired during a recovery nap after sleep deprivation in 20 young healthy participants (12 females, 8 males, age = 21.3 ± 2.5 years). Based on spindle events (onset and duration) detected by trained sleep scorers on BCG corrected EEG signals through a conventional average artefact subtraction (AAS) method, we compared four different EEG processing steps: non-BCG corrected; AAS BCG corrected; beamforming BCG corrected; beamforming+AAS BCG corrected. These processing steps consist of non-BCG corrected and AAS BCG corrected considered either at the sensor level or at the source-level (after beamformer localization) to evaluate the impact of the BCG artefact on the detection of spindle activity. Then we further investigated four different fMRI GLM approaches using 1) the spindle onset and duration (GLM1), 2) spindle onset, duration, and parametric modulation of single-spindle power change from the Cz electrode of the AAS BCG corrected data (GLM2), 3) spindle onset, duration, and parametric modulation of single-spindle power change from the beamforming+AAS BCG corrected (GLM3) and 4) spindle onset, duration, and parametric modulation of single-spindle power change from the beamforming BCG corrected data (GLM4). We found that the beamforming approach did not only attenuate the BCG artefacts, but also recovered sleep spindle activity occurring during NREM sleep. Furthermore, this beamforming approach allowed us to accurately estimate single-event power change of each spindle in the source space when compared to the channel level analysis, and therefore to further improve the specificity of fMRI GLM analysis, better localizing the recruited brain regions during spindles. Our findings show the benefit of applying beamforming source imaging technique to EEG-fMRI acquired during sleep. We demonstrate that this approach would be beneficial especially for long EEG-fMRI data acquisitions (i.e., sleep, resting-state), when the BCG correction becomes problematic due to inherent dynamic changes of heart rates. Our findings extend previous work regarding the application of the source imaging to the sleep EEG-fMRI. Combining with this advanced methodology and analysis, sleep EEG-fMRI will help us better understand the functional roles of human sleep.