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Paul Boon

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9 papers

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YNIMG Journal 2020 Journal Article

Localization of deep brain activity with scalp and subdural EEG

Mansoureh Fahimi Hnazaee
Benjamin Wittevrongel
Elvira Khachatryan
Arno Libert
Evelien Carrette
Ine Dauwe
Alfred Meurs
Paul Boon

To what extent electrocorticography (ECoG) and electroencephalography (scalp EEG) differ in their capability to locate sources of deep brain activity is far from evident. Compared to EEG, the spatial resolution and signal-to-noise ratio of ECoG is superior but its spatial coverage is more restricted, as is arguably the volume of tissue activity effectively measured from. Moreover, scalp EEG studies are providing evidence of locating activity from deep sources such as the hippocampus using high-density setups during quiet wakefulness. To address this question, we recorded a multimodal dataset from 4 patients with refractory epilepsy during quiet wakefulness. This data comprises simultaneous scalp, subdural and depth EEG electrode recordings. The latter was located in the hippocampus or insula and provided us with our “ground truth” for source localization of deep activity. We applied independent component analysis (ICA) for the purpose of separating the independent sources in theta, alpha and beta frequency band activity. In all patients subdural- and scalp EEG components were observed which had a significant zero-lag correlation with one or more contacts of the depth electrodes. Subsequent dipole modeling of the correlating components revealed dipole locations that were significantly closer to the depth electrodes compared to the dipole location of non-correlating components. These findings support the idea that components found in both recording modalities originate from neural activity in close proximity to the depth electrodes. Sources localized with subdural electrodes were ~70% closer to the depth electrode than sources localized with EEG with an absolute improvement of around ~2cm. In our opinion, this is not a considerable improvement in source localization accuracy given that, for clinical purposes, ECoG electrodes were implanted in close proximity to the depth electrodes. Furthermore, the ECoG grid attenuates the scalp EEG, due to the electrically isolating silastic sheets in which the ECoG electrodes are embedded. Our results on dipole modeling show that the deep source localization accuracy of scalp EEG is comparable to that of ECoG. Significance Statement Deep and subcortical regions play an important role in brain function. However, as joint recordings at multiple spatial scales to study brain function in humans are still scarce, it is still unresolved to what extent ECoG and EEG differ in their capability to locate sources of deep brain activity. To the best of our knowledge, this is the first study presenting a dataset of simultaneously recorded EEG, ECoG and depth electrodes in the hippocampus or insula, with a focus on non-epileptiform activity (quiet wakefulness). Furthermore, we are the first study to provide experimental findings on the comparison of source localization of deep cortical structures between invasive and non-invasive brain activity measured from the cortical surface.

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YNIMG Journal 2019 Journal Article

Alterations in the functional brain network in a rat model of epileptogenesis: A longitudinal resting state fMRI study

Emma Christiaen
Marie-Gabrielle Goossens
Robrecht Raedt
Benedicte Descamps
Lars Emil Larsen
Erine Craey
Evelien Carrette
Kristl Vonck

Epilepsy is a neurological disorder characterized by recurrent epileptic seizures. Electrophysiological and neuroimaging studies in patients with epilepsy suggest that abnormal functional brain networks play a role in the development of epilepsy, i. e. epileptogenesis, resulting in the generation of spontaneous seizures and cognitive impairment. In this longitudinal study, we investigated changes in functional brain networks during epileptogenesis in the intraperitoneal kainic acid (IPKA) rat model of temporal lobe epilepsy (TLE) using resting state functional magnetic resonance imaging (rsfMRI) and graph theory. Additionally, we investigated whether these changes are related to the frequency of occurrence of spontaneous epileptic seizures in the chronic phase of epilepsy. Using a 7T MRI system, rsfMRI images were acquired under medetomidine anaesthesia before and 1, 3, 6, 10 and 16 weeks after status epilepticus (SE) induction in 20 IPKA animals and 7 healthy control animals. To obtain a functional network, correlation between fMRI time series of 38 regions of interest (ROIs) was calculated. Then, several graph theoretical network measures were calculated to describe and quantify the network changes. At least 17 weeks post-SE, IPKA animals were implanted with electrodes in the left and right dorsal hippocampus, EEG was measured for 7 consecutive days and spontaneous seizures were counted. Our results show that correlation coefficients of fMRI time series shift to lower values during epileptogenesis, indicating weaker whole brain network connections. Segregation and integration in the functional brain network also decrease, indicating a lower local interconnectivity and a lower overall communication efficiency. Secondly, this study demonstrates that the largest decrease in functional connectivity is observed for the retrosplenial cortex. Finally, post-SE changes in functional connectivity, segregation and integration are correlated with seizure frequency in the IPKA rat model.

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YNIMG Journal 2019 Journal Article

Semantic and perceptual priming activate partially overlapping brain networks as revealed by direct cortical recordings in humans

Elvira Khachatryan
Benjamin Wittevrongel
Mansoureh Fahimi Hnazaee
Evelien Carrette
Ine Dauwe
Alfred Meurs
Paul Boon
Dirk Van Roost

Facilitation of object processing in the brain due to a related context (priming) can be influenced by both semantic connections and perceptual similarity. It is thus important to discern these two when evaluating the spatio-temporal dynamics of primed object processing. The repetition-priming paradigm frequently used to study perceptual priming is, however, unable to differentiate between the mentioned priming effects, possibly leading to confounded results. In the current study, we recorded brain signals from the scalp and cerebral convexity of nine patients with refractory epilepsy in response to related and unrelated image-pairs, all of which shared perceptual features while only related ones had a semantic connection. While previous studies employing a repetition-priming paradigm observed largely overlapping networks between semantic and perceptual priming effects, our results suggest that this overlap is only partial (both temporally and spatially). These findings stress the importance of controlling for perceptual features when studying semantic priming.

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YNIMG Journal 2018 Journal Article

Representation of steady-state visual evoked potentials elicited by luminance flicker in human occipital cortex: An electrocorticography study

Benjamin Wittevrongel
Elvira Khachatryan
Mansoureh Fahimi Hnazaee
Evelien Carrette
Leen De Taeye
Alfred Meurs
Paul Boon
Dirk Van Roost

Despite the widespread use of steady-state visual evoked potentials (SSVEPs) elicited by luminance flicker in clinical and research settings, their spatial and temporal representation in the occipital cortex largely remain elusive. We performed intracranial-EEG recordings in response to targets flickering at frequencies from 11 to 15 Hz using a subdural electrode grid covering the entire right occipital cortex of a human subject, and we were able to consistently locate the gazed stimulus frequency at the posterior side of the primary visual cortex (V1). Peripheral flickering, undetectable in scalp-EEG, elicited activations in the interhemispheric fissure at locations consistent with retinotopic maps. Both foveal and peripheral activations spatially coincided with activations in the high gamma band. We detected localized alpha synchronization at the lateral edge of V2 during stimulation and transient post-stimulation theta band activations at the posterior part of the occipital cortex. Scalp-EEG exhibited only a minor occipital post-stimulation theta activation, but a strong transient frontal activation.

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YNICL Journal 2017 Journal Article

EEG source connectivity to localize the seizure onset zone in patients with drug resistant epilepsy

Willeke Staljanssens
Gregor Strobbe
Roel Van Holen
Vincent Keereman
Stefanie Gadeyne
Evelien Carrette
Alfred Meurs
Francesca Pittau

Electrical source imaging (ESI) from interictal scalp EEG is increasingly validated and used as a valuable tool in the presurgical evaluation of epilepsy as a reflection of the irritative zone. ESI of ictal scalp EEG to localize the seizure onset zone (SOZ) remains challenging. We investigated the value of an approach for ictal imaging using ESI and functional connectivity analysis (FC). Ictal scalp EEG from 111 seizures in 27 patients who had Engel class I outcome at least 1year following resective surgery was analyzed. For every seizure, an artifact-free epoch close to the seizure onset was selected and ESI using LORETA was applied. In addition, the reconstructed sources underwent FC using the spectrum-weighted Adaptive Directed Transfer Function. This resulted in the estimation of the SOZ in two ways: (i) the source with maximal power after ESI, (ii) the source with the strongest outgoing connections after combined ESI and FC. Next, we calculated the distance between the estimated SOZ and the border of the resected zone (RZ) for both approaches and called this the localization error ((i) LEpow and (ii) LEconn respectively). By comparing LEpow and LEconn, we assessed the added value of FC. The source with maximal power after ESI was inside the RZ (LEpow =0mm) in 31% of the seizures and estimated within 10mm from the border of the RZ (LEpow ≤10mm) in 42%. Using ESI and FC, these numbers increased to 72% for LEconn =0mm and 94% for LEconn ≤10mm. FC provided a significant added value to ESI alone (p <0. 001). ESI combined with subsequent FC is able to localize the SOZ in a non-invasive way with high accuracy. Therefore it could be a valuable tool in the presurgical evaluation of epilepsy.

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YNICL Journal 2016 Journal Article

Electrical source imaging of interictal spikes using multiple sparse volumetric priors for presurgical epileptogenic focus localization

Gregor Strobbe
Evelien Carrette
José David López
Victoria Montes Restrepo
Dirk Van Roost
Alfred Meurs
Kristl Vonck
Paul Boon

Electrical source imaging of interictal spikes observed in EEG recordings of patients with refractory epilepsy provides useful information to localize the epileptogenic focus during the presurgical evaluation. However, the selection of the time points or time epochs of the spikes in order to estimate the origin of the activity remains a challenge. In this study, we consider a Bayesian EEG source imaging technique for distributed sources, i.e. the multiple volumetric sparse priors (MSVP) approach. The approach allows to estimate the time courses of the intensity of the sources corresponding with a specific time epoch of the spike. Based on presurgical averaged interictal spikes in six patients who were successfully treated with surgery, we estimated the time courses of the source intensities for three different time epochs: (i) an epoch starting 50 ms before the spike peak and ending at 50% of the spike peak during the rising phase of the spike, (ii) an epoch starting 50 ms before the spike peak and ending at the spike peak and (iii) an epoch containing the full spike time period starting 50 ms before the spike peak and ending 230 ms after the spike peak. To identify the primary source of the spike activity, the source with the maximum energy from 50 ms before the spike peak till 50% of the spike peak was subsequently selected for each of the time windows. For comparison, the activity at the spike peaks and at 50% of the peaks was localized using the LORETA inversion technique and an ECD approach. Both patient-specific spherical forward models and patient-specific 5-layered finite difference models were considered to evaluate the influence of the forward model. Based on the resected zones in each of the patients, extracted from post-operative MR images, we compared the distances to the resection border of the estimated activity. Using the spherical models, the distances to the resection border for the MSVP approach and each of the different time epochs were in the same range as the LORETA and ECD techniques. We found distances smaller than 23 mm, with robust results for all the patients. For the finite difference models, we found that the distances to the resection border for the MSVP inversions of the full spike time epochs were generally smaller compared to the MSVP inversions of the time epochs before the spike peak. The results also suggest that the inversions using the finite difference models resulted in slightly smaller distances to the resection border compared to the spherical models. The results we obtained are promising because the MSVP approach allows to study the network of the estimated source-intensities and allows to characterize the spatial extent of the underlying sources.

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YNICL Journal 2015 Journal Article

Network analysis of EEG related functional MRI changes due to medication withdrawal in focal epilepsy

Kees Hermans
Pauly Ossenblok
Petra van Houdt
Liesbeth Geerts
Rudolf Verdaasdonk
Paul Boon
Albert Colon
Jan C. de Munck

Anti-epileptic drugs (AEDs) have a global effect on the neurophysiology of the brain which is most likely reflected in functional brain activity recorded with EEG and fMRI. These effects may cause substantial inter-subject variability in studies where EEG correlated functional MRI (EEG-fMRI) is used to determine the epileptogenic zone in patients who are candidate for epilepsy surgery. In the present study the effects on resting state fMRI are quantified in conditions with AED administration and after withdrawal of AEDs. EEG-fMRI data were obtained from 10 patients in the condition that the patient was on the steady-state maintenance doses of AEDs as prescribed (condition A) and after withdrawal of AEDs (condition B), at the end of a clinically standard pre-surgical long term video-EEG monitoring session. Resting state networks (RSN) were extracted from fMRI. The epileptic component (ICE) was identified by selecting the RSN component with the largest overlap with the EEG-fMRI correlation pattern. Changes in RSN functional connectivity between conditions A and B were quantified. EEG-fMRI correlation analysis was successful in 30% and 100% of the cases in conditions A and B, respectively. Spatial patterns of ICEs are comparable in conditions A and B, except for one patient for whom it was not possible to identify the ICE in condition A. However, the resting state functional connectivity is significantly increased in the condition after withdrawal of AEDs (condition B), which makes resting state fMRI potentially a new tool to study AED effects. The difference in sensitivity of EEG-fMRI in conditions A and B, which is not related to the number of epileptic EEG events occurring during scanning, could be related to the increased functional connectivity in condition B.

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YNIMG Journal 2011 Journal Article

Accurate epileptogenic focus localization through time-variant functional connectivity analysis of intracranial electroencephalographic signals

Pieter van Mierlo
Evelien Carrette
Hans Hallez
Kristl Vonck
Dirk Van Roost
Paul Boon
Steven Staelens

Epilepsy is a neurological disorder characterized by seizures, i. e. abnormal synchronous activity of neurons in the brain. During a focal seizure, the abnormal synchronous activity starts in a specific brain region and rapidly propagates to neighboring regions. Intracranial ElectroEncephaloGraphy (IEEG) is the recording of brain activity at a high temporal resolution through electrodes placed within different brain regions. Intracranial electrodes are used to access structures deep within the brain and to reveal brain activity that cannot be observed with scalp EEG recordings. In order to identify the pattern of propagation across brain areas, a connectivity measure named the Adapted Directed Transfer Function (ADTF) has been developed. This measure reveals connections between different regions by exploiting statistical dependencies within multichannel recordings. The ADTF can be derived from the coefficients of a time-variant multivariate autoregressive (TVAR) model fitted to the data. In this paper the applicability to locate the epileptogenic focus by time-variant connectivity analysis of seizure onsets based on the ADTF is shown. Furthermore, different normalizations of the ADTF (the integrated ADTF, the masked ADTF and the full frequency ADTF) are compared to investigate whether one is more suitable to describe the spreading of epileptic activity during an epileptic seizure. We quantified the performance of different connectivity measures during simulations of an epileptic seizure onset. The full frequency ADTF outperforms the integrated ADTF and masked ADTF. Accordingly, we applied this full frequency ADTF to 4 seizure onset and 29 subclinical seizure IEEG recordings of a patient with refractory epilepsy. Hereby, we showed that connectivity patterns derived from IEEG recordings can provide useful information about seizure propagation and may improve the accuracy of the pre-surgical evaluation in patients with refractory epilepsy.

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YNIMG Journal 2010 Journal Article

Hippocampal deep brain stimulation induces decreased rCBF in the hippocampal formation of the rat

Tine Wyckhuys
Steven Staelens
Bregt Van Nieuwenhuyse
Steven Deleye
Hans Hallez
Kristl Vonck
Robrecht Raedt
Wytse Wadman

Deep brain stimulation (DBS) is a promising experimental approach to treat various neurological disorders. However, the optimal stimulation paradigm and the precise mechanism of action of DBS are unknown. Neuro-imaging by means of Single Photon Emission Computed Tomography (SPECT) is a non-invasive manner of evaluating regional cerebral blood flow (rCBF) changes, which are assumed to reflect changes in neural activity. In this study, rCBF changes induced by hippocampal DBS are evaluated by subtraction analysis of stimulation on/off using small animal µSPECT of the rat brain. Rats (n =13) were implanted with a multi-contact DBS electrode in the right hippocampus and injected with 10mCi of HMPAO-Tc99m during application of various hippocampal DBS paradigms and amplitudes and during sham stimulation. Subtraction analysis revealed that hippocampal DBS caused a significant decrease in relative rCBF, both in the ipsi- (the side of the implanted electrode) and contralateral hippocampus. Hypoperfusion spread contralaterally with increasing stimulation amplitude. A clear distinction in spatial extent and intensity of hypoperfusion was observed between stimulation paradigms: bipolar Poisson Distributed Stimulation induced significant hypoperfusion ipsi- and contralaterally (p <0. 01), while during other stimulation paradigms, rCBF-changes were less prominent. In conclusion, small animal µSPECT allows us to draw conclusions on the location, spatial extent and intensity of the hypoperfusion observed in the ipsi- and contralateral hippocampus, induced by hippocampal DBS. Our study demonstrates an innovative approach to visualize the effects of DBS and can be a useful tool in evaluating the effect of various stimulation paradigms and target areas for DBS.

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