EEG-fMRI Data Research Articles

Altered correlation of concurrently recorded EEG-fMRI connectomes in temporal lobe epilepsy.

Whole-brain functional connectivity networks (connectomes) have been characterized at different scales in humans using EEG and fMRI. Multimodal epileptic networks have also been investigated, but the relationship between EEG and fMRI defined networks on a whole-brain scale is unclear. A unified multimodal connectome description, mapping healthy and pathological networks would close this knowledge gap. Here, we characterize the spatial correlation between the EEG and fMRI connectomes in right and left temporal lobe epilepsy (rTLE/lTLE). From two centers, we acquired resting-state concurrent EEG-fMRI of 35 healthy controls and 34 TLE patients. EEG-fMRI data was projected into the Desikan brain atlas, and functional connectomes from both modalities were correlated. EEG and fMRI connectomes were moderately correlated. This correlation was increased in rTLE when compared to controls for EEG-delta/theta/alpha/beta. Conversely, multimodal correlation in lTLE was decreased in respect to controls for EEG-beta. While the alteration was global in rTLE, in lTLE it was locally linked to the default mode network. The increased multimodal correlation in rTLE and decreased correlation in lTLE suggests a modality-specific lateralized differential reorganization in TLE, which needs to be considered when comparing results from different modalities. Each modality provides distinct information, highlighting the benefit of multimodal assessment in epilepsy.

Robust memory of face moral values is encoded in the human caudate tail: a simultaneous EEG-fMRI study

Moral judgements about people based on their actions is a key component that guides social decision making. It is currently unknown how positive or negative moral judgments associated with a person’s face are processed and stored in the brain for a long time. Here, we investigate the long-term memory of moral values associated with human faces using simultaneous EEG-fMRI data acquisition. Results show that only a few exposures to morally charged stories of people are enough to form long-term memories a day later for a relatively large number of new faces. Event related potentials (ERPs) showed a significant differentiation of remembered good vs bad faces over centerofrontal electrode sites (value ERP). EEG-informed fMRI analysis revealed a subcortical cluster centered on the left caudate tail (CDt) as a correlate of the face value ERP. Importantly neither this analysis nor a conventional whole-brain analysis revealed any significant coding of face values in cortical areas, in particular the fusiform face area (FFA). Conversely an fMRI-informed EEG source localization using accurate subject-specific EEG head models also revealed activation in the left caudate tail. Nevertheless, the detected caudate tail region was found to be functionally connected to the FFA, suggesting FFA to be the source of face-specific information to CDt. A further psycho-physiological interaction analysis also revealed task-dependent coupling between CDt and dorsomedial prefrontal cortex (dmPFC), a region previously identified as retaining emotional working memories. These results identify CDt as a main site for encoding the long-term value memories of faces in humans suggesting that moral value of faces activates the same subcortical basal ganglia circuitry involved in processing reward value memory for objects in primates.

Heartbeat-evoked neural response abnormalities in generalized anxiety disorder during peripheral adrenergic stimulation.

Hyperarousal symptoms in generalized anxiety disorder (GAD) are often incongruent with the observed physiological state, suggesting that abnormal processing of interoceptive signals is a characteristic feature of the disorder. To examine the neural mechanisms underlying interoceptive dysfunction in GAD, we evaluated whether adrenergic modulation of cardiovascular signaling differentially affects the heartbeat-evoked potential (HEP), an electrophysiological marker of cardiac interoception, during concurrent electroencephalogram and functional magnetic resonance imaging (EEG-fMRI) scanning. Intravenous infusions of the peripheral adrenergic agonist isoproterenol (0.5 and 2.0 micrograms, μg) were administered in a randomized, double-blinded and placebo-controlled fashion to dynamically perturb the cardiovascular system while recording the associated EEG-fMRI responses. During the 0.5 μg isoproterenol infusion, the GAD group (n = 24) exhibited significantly larger changes in HEP amplitude in an opposite direction than the healthy comparison (HC) group (n = 24). In addition, the GAD group showed significantly larger absolute HEP amplitudes than theHC groupduring saline infusions, when cardiovascular tone did not increase. No significant group differences in HEP amplitude were identified during the 2.0 μg isoproterenol infusion. Using analyzable blood oxygenation level-dependent fMRI data from participants with concurrent EEG-fMRI data (21 GAD and 21 HC), we found that the aforementioned HEP effects were uncorrelated with fMRI signals in the insula, ventromedial prefrontal cortex, dorsal anterior cingulate cortex, amygdala, and somatosensory cortex, brain regions implicated in cardiac signal processing in prior fMRI studies. These findings provide additional evidence of dysfunctional cardiac interoception in GAD and identify neural processes at the electrophysiological level that may be independent from blood oxygen level-dependent responses during peripheral adrenergic stimulation.

Exploring changes in brain function in IBD patients using SPCCA: a study of simultaneous EEG-fMRI.

Research on functional changes in the brain of inflammatory bowel disease (IBD) patients is emerging around the world, which brings new perspectives to medical research. In this paper, the methods of canonical correlation analysis (CCA), kernel canonical correlation analysis (KCCA), and sparsity preserving canonical correlation analysis (SPCCA) were applied to the fusion of simultaneous EEG-fMRI data from 25 IBD patients and 15 healthy individuals. The CCA, KCCA and SPCCA fusion methods were used for data processing to compare the results obtained by the three methods. The results clearly show that there is a significant difference in the activation intensity between IBD and healthy control (HC), not only in the frontal lobe (p < 0.01) and temporal lobe (p < 0.01) regions, but also in the posterior cingulate gyrus (p < 0.01), gyrus rectus (p < 0.01), and amygdala (p < 0.01) regions, which are usually neglected. The mean difference in the SPCCA activation intensity was 60.1. However, the mean difference in activation intensity was only 36.9 and 49.8 by using CCA and KCCA. In addition, the correlation of the relevant components selected during the SPCCA calculation was high, with correlation components of up to 0.955; alternatively, the correlations obtained from CCA and KCCA calculations were only 0.917 and 0.926, respectively. It can be seen that SPCCA is indeed superior to CCA and KCCA in processing high-dimensional multimodal data. This work reveals the process of analyzing the brain activation state in IBD disease, provides a further perspective for the study of brain function, and opens up a new avenue for studying the SPCCA method and the change in the intensity of brain activation in IBD disease.

Insights from simultaneous EEG-fMRI and patient data illuminate the role of the anterior medial temporal lobe in N400 generation

The N400, a negative event-related potential (ERP) peaking approximately 400 ms after stimulus onset, is known to reflect the processing of semantic information. While scalp recordings have contributed to understanding the psychological processes underlying the N400, they have been limited in identifying its neural basis. However, recent intracranial ERP recordings and fMRI studies have shed light on the crucial role of the anterior medial temporal lobe (AMTL) in semantic information processing. These findings suggest that the N400 partially represents activity in the AMTL structures. To investigate the neural underpinnings of the N400 effect, we simultaneously recorded ERPs and event-related fMRI during a semantic priming paradigm in a sample of 12 young, healthy subjects. Additionally, we collected ERPs and structural brain data from older healthy adults and patients with amnestic mild cognitive impairment (aMCI), a population characterized by neurodegenerative changes in the AMTL. In our fMRI results, we identified bilateral loci in the AMTL as the global maxima. Employing an EEG-informed fMRI analysis, we explored trial-to-trial fluctuations in semantic processing by linking single-trial N400 amplitudes to the Blood Oxygen Level Dependent (BOLD) signal. This approach provided the first direct evidence linking the N400 recorded at the scalp level to the corresponding BOLD signal in the AMTL. Consistent with these findings, patients with aMCI exhibited a diminished N400 effect compared to healthy older adults. Furthermore, voxel-based morphometry analysis revealed a correlation between the magnitude of the N400 effect and the integrity of the AMTL. By integrating data from simultaneous EEG-fMRI, and patient studies, our research advances our understanding of the neural substrate of the N400 and highlights the critical involvement of the AMTL in semantic processing.

The role of middle frontal gyrus in working memory retrieval by the effect of target detection tasks: a simultaneous EEG-fMRI study.

Maintained working memory (WM) representations have been shown to influence visual target detection selection, while the effect of the visual target detection process on WM retrieval remains largely unknown. In the current research, we used the dual-paradigm of the visual target detection task and the delayed matching task (DMT), which contained the following four conditions: the match condition: the DMT target contained the detection target; the mismatch condition: the DMT target contained the detection distractor; the neutral condition: only the detection target was presented; the catch condition: only the DMT target was presented. Twenty-six subjects were recruited in the experiment with simultaneous EEG-fMRI data. Behaviorally, faster responses were found in the mismatch condition than in the match and neutral conditions. The EEG data found a greater parieto-occipital N1 component in the mismatch condition compared to the neutral condition, and a greater frontal N2 component in the match condition than in the mismatch condition. Moreover, compared to the match and neutral conditions, weaker activations of the bilateral middle frontal gyrus (MFG) were observed in the mismatch condition. And the representational similarity analysis (RSA) revealed significant differences in the representational patterns of the bilateral MFG between mismatch and match conditions, as well as in the representational patterns of the left MFG between mismatch and neutral conditions. Additionally, the left MFG may be the brain source of the N1 component in the mismatch condition. These findings suggest that the mismatch between the DMT target and detection target affects early attention allocation and attentional control in WM retrieval, and the MFG may play an important role in WM retrieval by the effect of the target detection task. In conclusion, our work deepens the understanding of the neural mechanisms by which visual target detection affects WM retrieval.

Decoding the temporal dynamics of affective scene processing

Natural images containing affective scenes are used extensively to investigate the neural mechanisms of visual emotion processing. Functional fMRI studies have shown that these images activate a large-scale distributed brain network that encompasses areas in visual, temporal, and frontal cortices. The underlying spatial and temporal dynamics, however, remain to be better characterized. We recorded simultaneous EEG-fMRI data while participants passively viewed affective images from the International Affective Picture System (IAPS). Applying multivariate pattern analysis to decode EEG data, and representational similarity analysis to fuse EEG data with simultaneously recorded fMRI data, we found that: (1) ∼80 ms after picture onset, perceptual processing of complex visual scenes began in early visual cortex, proceeding to ventral visual cortex at ∼100 ms, (2) between ∼200 and ∼300 ms (pleasant pictures: ∼200 ms; unpleasant pictures: ∼260 ms), affect-specific neural representations began to form, supported mainly by areas in occipital and temporal cortices, and (3) affect-specific neural representations were stable, lasting up to ∼2 s, and exhibited temporally generalizable activity patterns. These results suggest that affective scene representations in the brain are formed temporally in a valence-dependent manner and may be sustained by recurrent neural interactions among distributed brain areas.

A-PASS: an automated pipeline to analyze simultaneously acquired EEG-fMRI data for studying brain activities during sleep

Objective. Concurrent electroencephalography and functional magnetic resonance imaging (EEG-fMRI) signals can be used to uncover the nature of brain activities during sleep. However, analyzing simultaneously acquired EEG-fMRI data is extremely time consuming and experience dependent. Thus, we developed a pipeline, which we named A-PASS, to automatically analyze simultaneously acquired EEG-fMRI data for studying brain activities during sleep. Approach. A deep learning model was trained on a sleep EEG-fMRI dataset from 45 subjects and used to perform sleep stage scoring. Various fMRI indices can be calculated with A-PASS to depict the neurophysiological characteristics across different sleep stages. We tested the performance of A-PASS on an independent sleep EEG-fMRI dataset from 28 subjects. Statistical maps regarding the main effect of sleep stages and differences between each pair of stages of fMRI indices were generated and compared using both A-PASS and manual processing methods. Main results. The deep learning model implemented in A-PASS achieved both an accuracy and F1-score higher than 70% for sleep stage classification on EEG data acquired during fMRI scanning. The statistical maps generated from A-PASS largely resembled those produced from manually scored stages plus a combination of multiple software programs. Significance. A-PASS allowed efficient EEG-fMRI data processing without manual operation and could serve as a reliable and powerful tool for simultaneous EEG-fMRI studies on sleep.

Spatial signatures of anesthesia-induced burst-suppression differ between primates and rodents.

During deep anesthesia, the electroencephalographic (EEG) signal of the brain alternates between bursts of activity and periods of relative silence (suppressions). The origin of burst-suppression and its distribution across the brain remain matters of debate. In this work, we used functional magnetic resonance imaging (fMRI) to map the brain areas involved in anesthesia-induced burst-suppression across four mammalian species: humans, long-tailed macaques, common marmosets, and rats. At first, we determined the fMRI signatures of burst-suppression in human EEG-fMRI data. Applying this method to animal fMRI datasets, we found distinct burst-suppression signatures in all species. The burst-suppression maps revealed a marked inter-species difference: in rats, the entire neocortex engaged in burst-suppression, while in primates most sensory areas were excluded-predominantly the primary visual cortex. We anticipate that the identified species-specific fMRI signatures and whole-brain maps will guide future targeted studies investigating the cellular and molecular mechanisms of burst-suppression in unconscious states.

Modeling the Hemodynamic Response Function Using EEG-fMRI Data During Eyes-Open Resting-State Conditions and Motor Task Execution

Being able to accurately quantify the hemodynamic response function (HRF) that links the blood oxygen level dependent functional magnetic resonance imaging (BOLD-fMRI) signal to the underlying neural activity is important both for elucidating neurovascular coupling mechanisms and improving the accuracy of fMRI-based functional connectivity analyses. In particular, HRF estimation using BOLD-fMRI is challenging particularly in the case of resting-state data, due to the absence of information about the underlying neuronal dynamics. To this end, using simultaneously recorded electroencephalography (EEG) and fMRI data is a promising approach, as EEG provides a more direct measure of neural activations. In the present work, we employ simultaneous EEG-fMRI to investigate the regional characteristics of the HRF using measurements acquired during resting conditions. We propose a novel methodological approach based on combining distributed EEG source space reconstruction, which improves the spatial resolution of HRF estimation and using block-structured linear and nonlinear models, which enables us to simultaneously obtain HRF estimates and the contribution of different EEG frequency bands. Our results suggest that the dynamics of the resting-state BOLD signal can be sufficiently described using linear models and that the contribution of each band is region specific. Specifically, it was found that sensory-motor cortices exhibit positive HRF shapes, whereas the lateral occipital cortex and areas in the parietal cortex, such as the inferior and superior parietal lobule exhibit negative HRF shapes. To validate the proposed method, we repeated the analysis using simultaneous EEG-fMRI measurements acquired during execution of a unimanual hand-grip task. Our results reveal significant associations between BOLD signal variations and electrophysiological power fluctuations in the ipsilateral primary motor cortex, particularly for the EEG beta band, in agreement with previous studies in the literature.

EEG-fMRI: Ballistocardiogram Artifact Reduction by Surrogate Method for Improved Source Localization.

For the analysis of simultaneous EEG-fMRI recordings, it is vital to use effective artifact removal tools. This applies in particular to the ballistocardiogram (BCG) artifact which is difficult to remove without distorting signals of interest related to brain activity. Here, we documented the use of surrogate source models to separate the artifact-related signals from brain signals with minimal distortion of the brain activity of interest. The artifact topographies used for surrogate separation were created automatically using principal components analysis (PCA-S) or by manual selection of artifact components utilizing independent components analysis (ICA-S). Using real resting-state data from 55 subjects superimposed with simulated auditory evoked potentials (AEP), both approaches were compared with three established BCG artifact removal methods: Blind Source Separation (BSS), Optimal Basis Set (OBS), and a mixture of both (OBS-ICA). Each method was evaluated for its applicability for ERP and source analysis using the following criteria: the number of events surviving artifact threshold scans, signal-to-noise ratio (SNR), error of source localization, and signal variance explained by the dipolar model. Using these criteria, PCA-S and ICA-S fared best overall, with highly significant differences to the established methods, especially in source localization. The PCA-S approach was also applied to a single subject Berger experiment performed in the MRI scanner. Overall, the removal of BCG artifacts by the surrogate methods provides a substantial improvement for the analysis of simultaneous EEG-fMRI data compared to the established methods.

Optimizing EEG Source Reconstruction with Concurrent fMRI-Derived Spatial Priors

Reconstructing EEG sources involves a complex pipeline, with the inverse problem being the most challenging. Multiple inversion algorithms are being continuously developed, aiming to tackle the non-uniqueness of this problem, which has been shown to be partially circumvented by including prior information in the inverse models. Despite a few efforts, there are still current and persistent controversies regarding the inversion algorithm of choice and the optimal set of spatial priors to be included in the inversion models. The use of simultaneous EEG-fMRI data is one approach to tackle this problem. The spatial resolution of fMRI makes fMRI derived spatial priors very convenient for EEG reconstruction, however, only task activation maps and resting-state networks (RSNs) have been explored so far, overlooking the recent, but already accepted, notion that brain networks exhibit dynamic functional connectivity fluctuations. The lack of a systematic comparison between different source reconstruction algorithms, considering potentially more brain-informative priors such as fMRI, motivates the search for better reconstruction models. Using simultaneous EEG-fMRI data, here we compared four different inversion algorithms (minimum norm, MN; low resolution electromagnetic tomography, LORETA; empirical Bayes beamformer, EBB; and multiple sparse priors, MSP) under a Bayesian framework (as implemented in SPM), each with three different sets of priors consisting of: (1) those specific to the algorithm; (2) those specific to the algorithm plus fMRI task activation maps and RSNs; and (3) those specific to the algorithm plus fMRI task activation maps and RSNs and network modules of task-related dFC states estimated from the dFC fluctuations. The quality of the reconstructed EEG sources was quantified in terms of model-based metrics, namely the expectation of the posterior probability P(model|data) and variance explained of the inversion models, and the overlap/proportion of brain regions known to be involved in the visual perception tasks that the participants were submitted to, and RSN templates, with/within EEG source components. Model-based metrics suggested that model parsimony is preferred, with the combination MSP and priors specific to this algorithm exhibiting the best performance. However, optimal overlap/proportion values were found using EBB and priors specific to this algorithm and fMRI task activation maps and RSNs or MSP and considering all the priors (algorithm priors, fMRI task activation maps and RSNs and dFC state modules), respectively, indicating that fMRI spatial priors, including dFC state modules, might contain useful information to recover EEG source components reflecting neuronal activity of interest. Our main results show that providing fMRI spatial derived priors that reflect the dynamics of the brain might be useful to map neuronal activity more accurately from EEG-fMRI. Furthermore, this work paves the way towards a more informative selection of the optimal EEG source reconstruction approach, which may be critical in future studies.

Canonical EEG microstates transitions reflect switching among BOLD resting state networks and predict fMRI signal

Objective. Electroencephalography (EEG) microstates (MSs), which reflect a large topographical representation of coherent electrophysiological brain activity, are widely adopted to study cognitive processes mechanisms and aberrant alterations in brain disorders. MS topographies are quasi-stable lasting between 60–120 ms. Some evidence suggests that MS are the electrophysiological signature of resting-state networks (RSNs). However, the spatial and functional interpretation of MS and their association with functional magnetic resonance imaging (fMRI) remains unclear. Approach. In a cohort of healthy subjects (n = 52), we conducted several statistical and machine learning (ML) approaches analyses on the association among MS spatio-temporal dynamics and the blood-oxygenation-level dependent (BOLD) simultaneous EEG-fMRI data using statistical and ML approaches. Main results. Our results using a generalized linear model showed that MS transitions were largely and negatively associated with BOLD signals in the somatomotor, visual, dorsal attention, and ventral attention fMRI networks with limited association within the default mode network. Additionally, a novel recurrent neural network (RNN) confirmed the association between MS transitioning and fMRI signal while revealing that MS dynamics can model BOLD signals and vice versa. Significance. Results suggest that MS transitions may represent the deactivation of fMRI RSNs and provide evidence that both modalities measure common aspects of undergoing brain neuronal activities. These results may help to better understand the electrophysiological interpretation of MS.

Identification of Negative BOLD Responses in Epilepsy Using Windkessel Models.

Alongside positive blood oxygenation level–dependent (BOLD) responses associated with interictal epileptic discharges, a variety of negative BOLD responses (NBRs) are typically found in epileptic patients. Previous studies suggest that, in general, up to four mechanisms might underlie the genesis of NBRs in the brain: (i) neuronal disruption of network activity, (ii) altered balance of neurometabolic/vascular couplings, (iii) arterial blood stealing, and (iv) enhanced cortical inhibition. Detecting and classifying these mechanisms from BOLD signals are pivotal for the improvement of the specificity of the electroencephalography–functional magnetic resonance imaging (EEG-fMRI) image modality to identify the seizure-onset zones in refractory local epilepsy. This requires models with physiological interpretation that furnish the understanding of how these mechanisms are fingerprinted by their BOLD responses. Here, we used a Windkessel model with viscoelastic compliance/inductance in combination with dynamic models of both neuronal population activity and tissue/blood O2 to classify the hemodynamic response functions (HRFs) linked to the above mechanisms in the irritative zones of epileptic patients. First, we evaluated the most relevant imprints on the BOLD response caused by variations of key model parameters. Second, we demonstrated that a general linear model is enough to accurately represent the four different types of NBRs. Third, we tested the ability of a machine learning classifier, built from a simulated ensemble of HRFs, to predict the mechanism underlying the BOLD signal from irritative zones. Cross-validation indicates that these four mechanisms can be classified from realistic fMRI BOLD signals. To demonstrate proof of concept, we applied our methodology to EEG-fMRI data from five epileptic patients undergoing neurosurgery, suggesting the presence of some of these mechanisms. We concluded that a proper identification and interpretation of NBR mechanisms in epilepsy can be performed by combining general linear models and biophysically inspired models.

Functional connectivity between frontal/parietal regions and MTL–basal ganglia during feedback learning and declarative memory retrieval

Feedback assists the memory system in preserving the learnings from ongoing activities and updating it for future retrievals. Thus, the feedback coming from an individual's performance affects the behavior and, thereby, the performance. However, little is known regarding the interactions of learning and memory associated regions. Thus, we employ a combination of functional connectivity and neurovascular approach to explore the significance of these interactions. Our study comprises thirty-five volunteers who undergo a feedback declarative memory task using simultaneous EEG-fMRI data acquisition. Functional connectivity analysis showed that medial temporal lobe (MTL) and basal ganglia possess significant connectivity but differential relationships during feedback learning and memory retrieval. Specifically, Putamen and pallidum (sub-regions of basal ganglia) are the central hubs in these mechanisms. The neurovascular analysis reveals the increased correlation of frontal-alpha and theta powers with the bold activity of MTL during memory retrievals. The results also report the role of the frontal (and parietal) alpha-beta powers in de-synchronization (and synchronization) of the bold activity of caudate; and parietal-theta (frontal-higher-alpha) power in de-synchronization (and synchronization) of bold activity of right accumbens. Hence, the study demonstrates the significant role of the frontal-parietal EEG powers in MTL-basal ganglia relationships and neuronal adaptations during declarative memory retrieval.

EEG Signal Connectivity for Characterizing Interictal Activity in Patients With Mesial Temporal Lobe Epilepsy.

Over the last decade, several methods for analysis of epileptiform signals in electroencephalography (EEG) have been proposed. These methods mainly use EEG signal features in either the time or the frequency domain to separate regular, interictal, and ictal brain activity. The aim of this work was to evaluate the feasibility of using functional connectivity (FC) based feature extraction methods for the analysis of epileptiform discharges in EEG signals. These signals were obtained from EEG-fMRI sessions of 10 patients with mesial temporal lobe epilepsy (MTLE) with unilateral hippocampal atrophy. The connectivity functions investigated were motif synchronization, imaginary coherence, and magnitude squared coherence in the alpha, beta, and gamma bands of the EEG. EEG signals were sectioned into 1-s epochs and classified according to (using neurologist markers): activity far from interictal epileptiform discharges (IED), activity immediately before an IED and, finally, mid-IED activity. Connectivity matrices for each epoch for each FC function were built, and graph theory was used to obtain the following metrics: strength, cluster coefficient, betweenness centrality, eigenvector centrality (both local and global), and global efficiency. The statistical distributions of these metrics were compared among the three classes, using ANOVA, for each FC function. We found significant differences in all global (p < 0.001) and local (p < 0.00002) graph metrics of the far class compared with before and mid for motif synchronization on the beta band; local betweenness centrality also pointed to a degree of lateralization on the frontotemporal structures. This analysis demonstrates the potential of FC measures, computed using motif synchronization, for the characterization of epileptiform activity of MTLE patients. This methodology may be helpful in the analysis of EEG-fMRI data applied to epileptic foci localization. Nonetheless, the methods must be tested with a larger sample and with other epileptic phenotypes.

Data-driven beamforming technique to attenuate ballistocardiogram artefacts in electroencephalography-functional magnetic resonance imaging without detecting cardiac pulses in electrocardiography recordings.

Simultaneous recording of electroencephalography (EEG) and functional magnetic resonance imaging (fMRI) is a very promising non‐invasive neuroimaging technique. However, EEG data obtained from the simultaneous EEG–fMRI are strongly influenced by MRI‐related artefacts, namely gradient artefacts (GA) and ballistocardiogram (BCG) artefacts. When compared to the GA correction, the BCG correction is more challenging to remove due to its inherent variabilities and dynamic changes over time. The standard BCG correction (i.e., average artefact subtraction [AAS]), require detecting cardiac pulses from simultaneous electrocardiography (ECG) recording. However, ECG signals are also distorted and will become problematic for detecting reliable cardiac peaks. In this study, we focused on a beamforming spatial filtering technique to attenuate all unwanted source activities outside of the brain. Specifically, we applied the beamforming technique to attenuate the BCG artefact in EEG–fMRI, and also to recover meaningful task‐based neural signals during an attentional network task (ANT) which required participants to identify visual cues and respond accurately. We analysed EEG–fMRI data in 20 healthy participants during the ANT, and compared four different BCG corrections (non‐BCG corrected, AAS BCG corrected, beamforming + AAS BCG corrected, beamforming BCG corrected). We demonstrated that the beamforming approach did not only significantly reduce the BCG artefacts, but also significantly recovered the expected task‐based brain activity when compared to the standard AAS correction. This data‐driven beamforming technique appears promising especially for longer data acquisition of sleep and resting EEG–fMRI. Our findings extend previous work regarding the recovery of meaningful EEG signals by an optimized suppression of MRI‐related artefacts.

Localization of Epileptic Foci Based on Simultaneous EEG–fMRI Data

Combining functional magnetic resonance imaging (fMRI) and electroencephalography (EEG) enables a non-invasive investigation of the human brain function and evaluation of the correlation of these two important modalities of brain activity. This paper explores recent reports on using advanced simultaneous EEG–fMRI methods proposed to map the regions and networks involved in focal epileptic seizure generation. One of the applications of EEG and fMRI combination as a valuable clinical approach is the pre-surgical evaluation of patients with epilepsy to map and localize the precise brain regions associated with epileptiform activity. In the process of conventional analysis using EEG–fMRI data, the interictal epileptiform discharges (IEDs) are visually extracted from the EEG data to be convolved as binary events with a predefined hemodynamic response function (HRF) to provide a model of epileptiform BOLD activity and use as a regressor for general linear model (GLM) analysis of the fMRI data. This review examines the methodologies involved in performing such studies, including techniques used for the recording of EEG inside the scanner, artifact removal, and statistical analysis of the fMRI signal. It then discusses the results reported for patients with primary generalized epilepsy and patients with different types of focal epileptic disorders. An important matter that these results have brought to light is that the brain regions affected by interictal epileptic discharges might not be limited to the ones where they have been generated. The developed methods can help reveal the regions involved in or affected by a seizure onset zone (SOZ). As confirmed by the reviewed literature, EEG–fMRI provides information that comes particularly useful when evaluating patients with refractory epilepsy for surgery.

Localization of interictal discharge origin: A simultaneous intracranial electroencephalographic-functional magnetic resonance imaging study.

Scalp electroencephalographic (EEG)-functional magnetic resonance imaging (fMRI) studies suggest that the maximum blood oxygen level-dependent (BOLD) response to an interictal epileptiform discharge (IED) identifies the area of IED generation. However, the maximum BOLD response has also been reported in distant, seemingly irrelevant areas. Given the poor postoperative outcomes associated with extra-temporal lobe epilepsy, we hypothesized this finding is more common when analyzing extratemporal IEDs as compared to temporal IEDs. We further hypothesized that a subjective, holistic assessment of other significant BOLD clusters to identify the most clinically relevant cluster could be used to overcome this limitation and therefore better identify the likely origin of an IED. Specifically, we also considered the second maximum cluster and the cluster closest to the electrode contacts where the IED was observed. Maps of significant IED-related BOLD activation were generated for 48 different IEDs recorded from 33 patients who underwent intracranial EEG-fMRI. The locations of the maximum, second maximum, and closest clusters were identified for each IED. An epileptologist, blinded to these cluster assignments, selected the most clinically relevant BOLD cluster, taking into account all available clinical information. The distances between these BOLD clusters and their corresponding IEDs were then measured. The most clinically relevant cluster was the maximum cluster for 56% (27/48) of IEDs, the second maximum cluster for 13% (6/48) of IEDs, and the closest cluster for 31% (15/48) of IEDs. The maximum clusters were closer to IED contacts for temporal than for extratemporal IEDs (p=.022), whereas the most clinically relevant clusters were not significantly different (p=.056). The maximum BOLD response to IEDs may not always be the most indicative of IED origin. We propose that available clinical information should be used in conjunction with EEG-fMRI data to identify a BOLD cluster representative of the IED origin.

Augmenting interictal mapping with neurovascular coupling biomarkers by structured factorization of epileptic EEG and fMRI data

EEG-correlated fMRI analysis is widely used to detect regional BOLD fluctuations that are synchronized to interictal epileptic discharges, which can provide evidence for localizing the ictal onset zone. However, the typical, asymmetrical and mass-univariate approach cannot capture the inherent, higher order structure in the EEG data, nor multivariate relations in the fMRI data, and it is nontrivial to accurately handle varying neurovascular coupling over patients and brain regions. We aim to overcome these drawbacks in a data-driven manner by means of a novel structured matrix-tensor factorization: the single-subject EEG data (represented as a third-order spectrogram tensor) and fMRI data (represented as a spatiotemporal BOLD signal matrix) are jointly decomposed into a superposition of several sources, characterized by space-time-frequency profiles. In the shared temporal mode, Toeplitz-structured factors account for a spatially specific, neurovascular ‘bridge’ between the EEG and fMRI temporal fluctuations, capturing the hemodynamic response’s variability over brain regions. By analyzing interictal data from twelve patients, we show that the extracted source signatures provide a sensitive localization of the ictal onset zone (10/12). Moreover, complementary parts of the IOZ can be uncovered by inspecting those regions with the most deviant neurovascular coupling, as quantified by two entropy-like metrics of the hemodynamic response function waveforms (9/12). Hence, this multivariate, multimodal factorization provides two useful sets of EEG-fMRI biomarkers, which can assist the presurgical evaluation of epilepsy. We make all code required to perform the computations available at https://github.com/svaneynd/structured-cmtf.