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Exploring the advantages of multiband fMRI with simultaneous EEG to investigate coupling between gamma frequency neural activity and the BOLD response in humans.

ABSTRACT: We established an optimal combination of EEG recording during sparse multiband (MB) fMRI that preserves high-resolution, whole-brain fMRI coverage while enabling broad-band EEG recordings which are uncorrupted by MRI gradient artefacts (GAs). We first determined the safety of simultaneous EEG recording during MB fMRI. Application of MB factor?=?4 produced <1°C peak heating of electrode/hardware during 20 min of GE-EPI data acquisition. However, higher SAR sequences require specific safety testing, with greater heating observed using PCASL with MB factor?=?4. Heating was greatest in the electrocardiogram channel, likely due to it possessing longest lead length. We investigated the effect of MB factor on the temporal signal-to-noise ratio for a range of GE-EPI sequences (varying MB factor and temporal interval between slice acquisitions). We found that, for our experimental purpose, the optimal acquisition was achieved with MB factor?=?3, 3mm isotropic voxels, and 33 slices providing whole head coverage. This sequence afforded a 2.25 s duration quiet period (without GAs) in every 3 s TR. Using this sequence, we demonstrated the ability to record gamma frequency (55-80 Hz) EEG oscillations, in response to right index finger abduction, that are usually obscured by GAs during continuous fMRI data acquisition. In this novel application of EEG-MB fMRI to a motor task, we observed a positive correlation between gamma and BOLD responses in bilateral motor regions. These findings support and extend previous work regarding coupling between neural and hemodynamic measures of brain activity in humans and showcase the utility of EEG-MB fMRI for future investigations.

SUBMITTER: Uji M

PROVIDER: S-EPMC6866630 | biostudies-literature | 2018 Apr

REPOSITORIES: biostudies-literature

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Exploring the advantages of multiband fMRI with simultaneous EEG to investigate coupling between gamma frequency neural activity and the BOLD response in humans.

Uji Makoto M Wilson Ross R Francis Susan T ST Mullinger Karen J KJ Mayhew Stephen D SD

Human brain mapping 20180113 4

We established an optimal combination of EEG recording during sparse multiband (MB) fMRI that preserves high-resolution, whole-brain fMRI coverage while enabling broad-band EEG recordings which are uncorrupted by MRI gradient artefacts (GAs). We first determined the safety of simultaneous EEG recording during MB fMRI. Application of MB factor = 4 produced <1°C peak heating of electrode/hardware during 20 min of GE-EPI data acquisition. However, higher SAR sequences require specific safety testin ...[more]

PMID: 29331056

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Project description:ObjectivesSimultaneous intracranial EEG and functional MRI (icEEG-fMRI) can be used to map the haemodynamic (BOLD) changes associated with the generation of IEDs. Unlike scalp EEG-fMRI, in most patients who undergo icEEG-fMRI, IEDs recorded intracranially are numerous and show variability in terms of field amplitude and morphology. Therefore, visual marking can be highly subjective and time consuming. In this study, we applied an automated spike classification algorithm, Wave_clus (WC), to IEDs marked visually on icEEG data acquired during simultaneous fMRI acquisition. The motivation of this work is to determine whether using a potentially more consistent and unbiased automated approach can produce more biologically meaningful BOLD patterns compared to the BOLD patterns obtained based on the conventional, visual classification.MethodsWe analysed simultaneous icEEG-fMRI data from eight patients with severe drug resistant epilepsy, and who subsequently underwent resective surgery that resulted in a good outcome: confirmed epileptogenic zone (EZ). For each patient two fMRI analyses were performed: one based on the conventional visual IED classification and the other based on the automated classification. We used the concordance of the IED-related BOLD maps with the confirmed EZ as an indication of their biological meaning, which we compared for the automated and visual classifications for all IED originating in the EZ.ResultsAcross the group, the visual and automated classifications resulted in 32 and 24 EZ IED classes respectively, for which 75% vs 83% of the corresponding BOLD maps were concordant. At the single-subject level, the BOLD maps for the automated approach had greater concordance in four patients, and less concordance in one patient, compared to those obtained using the conventional visual classification, and equal concordance for three remaining patients. These differences did not reach statistical significance.ConclusionWe found automated IED classification on icEEG data recorded during fMRI to be feasible and to result in IED-related BOLD maps that may contain similar or greater biological meaning compared to the conventional approach in the majority of the cases studied. We anticipate that this approach will help to gain significant new insights into the brain networks associated with IEDs and in relation to postsurgical outcome.

Project description:BackgroundEEG studies of working memory (WM) have demonstrated load dependent frequency band modulations. FMRI studies have localized load modulated activity to the dorsolateral prefrontal cortex (DLPFC), medial prefrontal cortex (MPFC), and posterior parietal cortex (PPC). Recently, an EEG-fMRI study found that low frequency band (theta and alpha) activity negatively correlated with the BOLD signal during the retention phase of a WM task. However, the coupling of higher (beta and gamma) frequencies with the BOLD signal during WM is unknown.MethodologyIn 16 healthy adult subjects, we first investigated EEG-BOLD signal correlations for theta (5-7 Hz), alpha1 (8-10), alpha2 (10-12 Hz), beta1 (13-20), beta2 (20-30 Hz), and gamma (30-40 Hz) during the retention period of a WM task with set size 2 and 5. Secondly, we investigated whether load sensitive brain regions are characterised by effects that relate frequency bands to BOLD signals effects.Principal findingsWe found negative theta-BOLD signal correlations in the MPFC, PPC, and cingulate cortex (ACC and PCC). For alpha1 positive correlations with the BOLD signal were found in ACC, MPFC, and PCC; negative correlations were observed in DLPFC, PPC, and inferior frontal gyrus (IFG). Negative alpha2-BOLD signal correlations were observed in parieto-occipital regions. Beta1-BOLD signal correlations were positive in ACC and negative in precentral and superior temporal gyrus. Beta2 and gamma showed only positive correlations with BOLD, e.g., in DLPFC, MPFC (gamma) and IFG (beta2/gamma). The load analysis revealed that theta and--with one exception--beta and gamma demonstrated exclusively positive load effects, while alpha1 showed only negative effects.ConclusionsWe conclude that the directions of EEG-BOLD signal correlations vary across brain regions and EEG frequency bands. In addition, some brain regions show both load sensitive BOLD and frequency band effects. Our data indicate that lower as well as higher frequency brain oscillations are linked to neurovascular processes during WM.

Project description:Simultaneous resting state functional magnetic resonance imaging (rsfMRI)-resting state electroencephalography (rsEEG) studies in healthy adults showed robust positive associations of signal power in the alpha band with BOLD signal in the thalamus, and more heterogeneous associations in cortical default mode network (DMN) regions. Negative associations were found in occipital regions. In Alzheimer's disease (AD), rsfMRI studies revealed a disruption of the DMN, while rsEEG studies consistently reported a reduced power within the alpha band. The present study is the first to employ simultaneous rsfMRI-rsEEG in an AD sample, investigating the association of alpha band power and BOLD signal, compared to healthy controls (HC). We hypothesized to find reduced positive associations in DMN regions and reduced negative associations in occipital regions in the AD group. Simultaneous resting state fMRI-EEG was recorded in 14 patients with mild AD and 14 HC, matched for age and gender. Power within the EEG alpha band (8-12 Hz, 8-10 Hz, and 10-12 Hz) was computed from occipital electrodes and served as regressor in voxel-wise linear regression analyses, to assess the association with the BOLD signal. Compared to HC, the AD group showed significantly decreased positive associations between BOLD signal and occipital alpha band power in clusters in the superior, middle and inferior frontal cortex, inferior temporal lobe and thalamus (p < 0.01, uncorr., cluster size ≥ 50 voxels). This group effect was more pronounced in the upper alpha sub-band, compared to the lower alpha sub-band. Notably, we observed a high inter-individual heterogeneity. Negative associations were only reduced in the lower alpha range in the hippocampus, putamen and cerebellum. The present study gives first insights into the relationship of resting-state EEG and fMRI characteristics in an AD sample. The results suggest that positive associations between alpha band power and BOLD signal in numerous regions, including DMN regions, are diminished in AD.

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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Exploring the advantages of multiband fMRI with simultaneous EEG to investigate coupling between gamma frequency neural activity and the BOLD response in humans.

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Exploring the advantages of multiband fMRI with simultaneous EEG to investigate coupling between gamma frequency neural activity and the BOLD response in humans.

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