Dataset Information

Pushing the Limits of EEG: Estimation of Large-Scale Functional Brain Networks and Their Dynamics Validated by Simultaneous fMRI.

ABSTRACT: Functional magnetic resonance imaging (fMRI) is the technique of choice for detecting large-scale functional brain networks and to investigate their dynamics. Because fMRI measures brain activity indirectly, electroencephalography (EEG) has been recently considered a feasible tool for detecting such networks, particularly the resting-state networks (RSNs). However, a truly unbiased validation of such claims is still missing, which can only be accomplished by using simultaneously acquired EEG and fMRI data, due to the spontaneous nature of the activity underlying the RSNs. Additionally, EEG is still poorly explored for the purpose of mapping task-specific networks, and no studies so far have been focused on investigating networks' dynamic functional connectivity (dFC) with EEG. Here, we started by validating RSNs derived from the continuous reconstruction of EEG sources by directly comparing them with those derived from simultaneous fMRI data of 10 healthy participants, and obtaining an average overlap (quantified by the Dice coefficient) of 0.4. We also showed the ability of EEG to map the facial expressions processing network (FEPN), highlighting regions near the posterior superior temporal sulcus, where the FEPN is anchored. Then, we measured the dFC using EEG for the first time in this context, estimated dFC brain states using dictionary learning, and compared such states with those obtained from the fMRI. We found a statistically significant match between fMRI and EEG dFC states, and determined the existence of two matched dFC states which contribution over time was associated with the brain activity at the FEPN, showing that the dynamics of FEPN can be captured by both fMRI and EEG. Our results push the limits of EEG toward being used as a brain imaging tool, while supporting the growing literature on EEG correlates of (dynamic) functional connectivity measured with fMRI, and providing novel insights into the coupling mechanisms underlying the two imaging techniques.

SUBMITTER: Abreu R

PROVIDER: S-EPMC7177188 | biostudies-literature | 2020

REPOSITORIES: biostudies-literature

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Pushing the Limits of EEG: Estimation of Large-Scale Functional Brain Networks and Their Dynamics Validated by Simultaneous fMRI.

Abreu Rodolfo R Abreu Rodolfo R Simões Marco M Castelo-Branco Miguel M

Frontiers in neuroscience 20200416

Functional magnetic resonance imaging (fMRI) is the technique of choice for detecting large-scale functional brain networks and to investigate their dynamics. Because fMRI measures brain activity indirectly, electroencephalography (EEG) has been recently considered a feasible tool for detecting such networks, particularly the resting-state networks (RSNs). However, a truly unbiased validation of such claims is still missing, which can only be accomplished by using simultaneously acquired EEG and ...[more]

PMID: 32372908

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Project description:Background: Potentially curative epilepsy surgery can be offered if a single, discrete epileptogenic zone (EZ) can be identified. For individuals in whom there is no clear concordance between clinical localization, scalp EEG, and imaging data, intracranial EEG (icEEG) may be needed to confirm a predefined hypothesis regarding irritative zone (IZ), seizure onset zone (SOZ), and EZ prior to surgery. However, icEEG has limited spatial sampling and may fail to reveal the full extent of epileptogenic network if predefined hypothesis is not correct. Simultaneous icEEG-fMRI has been safely acquired in humans and allows exploration of neuronal activity at the whole-brain level related to interictal epileptiform discharges (IED) captured intracranially. Methods: We report icEEG-fMRI in eight patients with refractory focal epilepsy who had resective surgery and good postsurgical outcome. Surgical resection volume in seizure-free patients post-surgically reflects confirmed identification of the EZ. IEDs on icEEG were classified according to their topographic distribution and localization (Focal, Regional, Widespread, and Non-contiguous). We also divided IEDs by their location within the surgical resection volume [primary IZ (IZ1) IED] or outside [secondary IZ (IZ2) IED]. The distribution of fMRI blood oxygen level-dependent (BOLD) changes associated with individual IED classes were assessed over the whole brain using a general linear model. The concordance of resulting BOLD map was evaluated by comparing localization of BOLD clusters with surgical resection volume. Additionally, we compared the concordance of BOLD maps and presence of BOLD clusters in remote brain areas: precuneus, cuneus, cingulate, medial frontal, and thalamus for different IED classes. Results: A total of 38 different topographic IED classes were identified across the 8 patients: Focal (22) and non-focal (16, Regional = 9, Widespread = 2, Non-contiguous = 5). Twenty-nine IEDs originated from IZ1 and 9 from IZ2. All IED classes were associated with BOLD changes. BOLD maps were concordant with the surgical resection volume for 27/38 (71%) IED classes, showing statistical global maximum BOLD cluster or another cluster in the surgical resection volume. The concordance of BOLD maps with surgical resection volume was greater (p < 0.05) for non-focal (87.5%, 14/16) as compared to Focal (59%, 13/22) IED classes. Additionally, BOLD clusters in remote cortical and deep brain areas were present in 84% (32/38) of BOLD maps, more commonly (15/16; 93%) for non-focal IED-related BOLD maps. Conclusions: Simultaneous icEEG-fMRI can reveal BOLD changes at the whole-brain level for a wide range of IEDs on icEEG. BOLD clusters within surgical resection volume and remote brain areas were more commonly seen for non-focal IED classes, suggesting that a wider hemodynamic network is at play.

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Project description:Epileptic networks, defined as brain regions involved in epileptic brain activity, have been mapped by functional connectivity in simultaneous electroencephalography and functional magnetic resonance imaging (EEG-fMRI) recordings. This technique allows to define brain hemodynamic changes, measured by the Blood Oxygen Level Dependent (BOLD) signal, associated to the interictal epileptic discharges (IED), which together with ictal events constitute a signature of epileptic disease. Given the highly time-varying nature of epileptic activity, a dynamic functional connectivity (dFC) analysis of EEG-fMRI data appears particularly suitable, having the potential to identify transitory features of specific connections in epileptic networks. In the present study, we propose a novel method, defined dFC-EEG, that integrates dFC assessed by fMRI with the information recorded by simultaneous scalp EEG, in order to identify the connections characterised by a dynamic profile correlated with the occurrence of IED, forming the dynamic epileptic subnetwork. Ten patients with drug-resistant focal epilepsy were included, with different aetiology and showing a widespread (or multilobar) BOLD activation, defined as involving at least two distinct clusters, located in two different lobes and/or extended to the hemisphere contralateral to the epileptic focus. The epileptic focus was defined from the IED-related BOLD map. Regions involved in the occurrence of interictal epileptic activity; i.e., forming the epileptic network, were identified by a general linear model considering the timecourse of the fMRI-defined focus as main regressor. dFC between these regions was assessed with a sliding-window approach. dFC timecourses were then correlated with the sliding-window variance of the IED signal (VarIED), to identify connections whose dynamics related to the epileptic activity; i.e., the dynamic epileptic subnetwork. As expected, given the very different clinical picture of each individual, the extent of this subnetwork was highly variable across patients, but was but was reduced of at least 30% with respect to the initially identified epileptic network in 9/10 patients. The connections of the dynamic subnetwork were most commonly close to the epileptic focus, as reflected by the laterality index of the subnetwork connections, reported higher than the one within the original epileptic network. Moreover, the correlation between dFC timecourses and VarIED was predominantly positive, suggesting a strengthening of the dynamic subnetwork associated to the occurrence of IED. The integration of dFC and scalp IED offers a more specific description of the epileptic network, identifying connections strongly influenced by IED. These findings could be relevant in the pre-surgical evaluation for the resection or disconnection of the epileptogenic zone and help in reaching a better post-surgical outcome. This would be particularly important for patients characterised by a widespread pathological brain activity which challenges the surgical intervention.

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Dataset Information

Pushing the Limits of EEG: Estimation of Large-Scale Functional Brain Networks and Their Dynamics Validated by Simultaneous fMRI.

Publications

Pushing the Limits of EEG: Estimation of Large-Scale Functional Brain Networks and Their Dynamics Validated by Simultaneous fMRI.

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