Abstract
In this study, we aimed to demonstrate whether spontaneous fluctuations in the blood oxygen level dependent (BOLD) signal derived from resting state functional magnetic resonance imaging (fMRI) reflect spontaneous neuronal activity in pathological brain regions as well as in regions spared by epileptiform discharges. This is a crucial issue as coherent fluctuations of fMRI signals between remote brain areas are now widely used to define functional connectivity in physiology and in pathophysiology. We quantified functional connectivity using non-linear measures of cross-correlation between signals obtained from intracerebral EEG (iEEG) and resting-state functional MRI (fMRI) in 5 patients suffering from intractable temporal lobe epilepsy (TLE). Functional connectivity was quantified with both modalities in areas exhibiting different electrophysiological states (epileptic and non affected regions) during the interictal period. Functional connectivity as measured from the iEEG signal was higher in regions affected by electrical epileptiform abnormalities relative to non-affected areas, whereas an opposite pattern was found for functional connectivity measured from the BOLD signal. Significant negative correlations were found between the functional connectivities of iEEG and BOLD signal when considering all pairs of signals (theta, alpha, beta and broadband) and when considering pairs of signals in regions spared by epileptiform discharges (in broadband signal). This suggests differential effects of epileptic phenomena on electrophysiological and hemodynamic signals and/or an alteration of the neurovascular coupling secondary to pathological plasticity in TLE even in regions spared by epileptiform discharges. In addition, indices of directionality calculated from both modalities were consistent showing that the epileptogenic regions exert a significant influence onto the non epileptic areas during the interictal period. This study shows that functional connectivity measured by iEEG and BOLD signals give complementary but sometimes inconsistent information in TLE.
Highlights
It has been largely demonstrated that a coherent slow fluctuation in blood-oxygen-level-dependent (BOLD) signals at rest is an accurate signature of functional connectivity between remote brain areas [1,2,3]
In this study, we aimed to investigate the relationship between BOLD and intracerebral EEG (iEEG) signals by comparing the functional connectivity calculated based on the two types of data in epileptic areas and regions spared by epileptiform activities during the interictal state in 5 patients with temporal lobe epilepsy (TLE), the commonest form of partial epilepsies
Classification of the regions of interest according to the epileptic process We identified regions of interest (ROI) for each patient representative of EZ/IZ1, IZ2 or NIZ based on both ictal and interictal iEEG data and the position of the labeled iEEG electrode contacts
Summary
It has been largely demonstrated that a coherent slow fluctuation in blood-oxygen-level-dependent (BOLD) signals at rest is an accurate signature of functional connectivity between remote brain areas [1,2,3]. Using simultaneous BOLD and intracortical electrophysiological signal recordings of visual cortices of monkeys, Shmuel & Leopold were the first to show a correlation between slow fluctuations in BOLD signals and the underlying local neuronal activity in healthy animals [4] In humans, He and colleagues have demonstrated a correlation structure between spontaneous BOLD fluctuations and slow cortical potentials (,4 Hz) recorded by electrocorticography (ECoG) in 5 patients during presurgical evaluation of drugresistant partial epilepsies [5]. To date, no data are available concerning the electrophysiological correlates of BOLD signal fluctuations in structures exhibiting epileptiform discharges This issue is of crucial interest to test the clinical relevance of resting-state fMRI in the presurgical assessment of intractable epilepsies and to better understand the functional alterations associated with these pathologies. In previous studies we demonstrated decreased functional connectivity as measured by resting-state fMRI in epileptic regions, contrasting with a global increase of functional connectivity as measured by intracerebral EEG (iEEG) recording using stereo-electroencephalography (SEEG) [10,11,13]
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