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      Interictal Functional Connectivity of Human Epileptic Networks Assessed by Intracerebral EEG and BOLD Signal Fluctuations

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          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.

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          Most cited references34

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          Functional connectivity in single and multislice echoplanar imaging using resting-state fluctuations.

          A previous report of correlations in low-frequency resting-state fluctuations between right and left hemisphere motor cortices in rapidly sampled single-slice echoplanar data is confirmed using a whole-body echoplanar MRI scanner at 1.5 T. These correlations are extended to lower sampling rate multislice echoplanar acquisitions and other right/left hemisphere-symmetric functional cortices. The specificity of the correlations in the lower sampling-rate acquisitions is lower due to cardiac and respiratory-cycle effects which are aliased into the pass-band of the low-pass filter. Data are combined for three normal right-handed male subjects. Correlations to left hemisphere motor cortex, visual cortex, and amygdala are measured in long resting-state scans.
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            Coupling between neuronal firing, field potentials, and FMRI in human auditory cortex.

            Functional magnetic resonance imaging (fMRI) is an important tool for investigating human brain function, but the relationship between the hemodynamically based fMRI signals in the human brain and the underlying neuronal activity is unclear. We recorded single unit activity and local field potentials in auditory cortex of two neurosurgical patients and compared them with the fMRI signals of 11 healthy subjects during presentation of an identical movie segment. The predicted fMRI signals derived from single units and the measured fMRI signals from auditory cortex showed a highly significant correlation (r = 0.75, P < 10(-47)). Thus, fMRI signals can provide a reliable measure of the firing rate of human cortical neurons.
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              Negative functional MRI response correlates with decreases in neuronal activity in monkey visual area V1.

              Most functional brain imaging studies use task-induced hemodynamic responses to infer underlying changes in neuronal activity. In addition to increases in cerebral blood flow and blood oxygenation level-dependent (BOLD) signals, sustained negative responses are pervasive in functional imaging. The origin of negative responses and their relationship to neural activity remain poorly understood. Through simultaneous functional magnetic resonance imaging and electrophysiological recording, we demonstrate a negative BOLD response (NBR) beyond the stimulated regions of visual cortex, associated with local decreases in neuronal activity below spontaneous activity, detected 7.15 +/- 3.14 mm away from the closest positively responding region in V1. Trial-by-trial amplitude fluctuations revealed tight coupling between the NBR and neuronal activity decreases. The NBR was associated with comparable decreases in local field potentials and multiunit activity. Our findings indicate that a significant component of the NBR originates in neuronal activity decreases.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2011
                19 May 2011
                : 6
                : 5
                : e20071
                Affiliations
                [1 ]CNRS (Centre National de la Recherche Scientifique), UMR 6612, CRMBM (Centre de Résonance Magnétique Biologique et Médicale), Marseille, France
                [2 ]INSERM (Institut National de la Santé et de la Recherche Médicale), U751, Laboratoire de Neurophysiologie et Neuropsychologie, Marseille, France
                [3 ]Université de la Méditerranée Aix-Marseille II, Faculté de Médecine, Marseille, France
                [4 ]Pôle d'imagerie Médicale, Assistance Publique – Hôpitaux de Marseille, Marseille, France
                [5 ]Pôle de Neurosciences Cliniques, Assistance Publique – Hôpitaux de Marseille, Marseille, France
                [6 ]INSERM (Institut National de la Santé et de la Recherche Médicale), U642, Rennes, France
                [7 ]UCL (University College London), Department of Clinical and Experimental Epilepsy, UCL Institute of Neurology, London, United Kingdom
                [8 ]MRI Unit, National Society for Epilepsy, Buckinghamshire, United Kingdom
                Consejo Superior de Investigaciones Cientificas - Instituto Cajal, Spain
                Author notes

                Conceived and designed the experiments: GB MG FB J-PR SC-G. Performed the experiments: GB MG J-PR. Analyzed the data: GB J-PR FB FW. Contributed reagents/materials/analysis tools: GB FW CGB JR. Wrote the paper: GB MG FB J-PR LL PC PJC.

                Article
                PONE-D-10-03624
                10.1371/journal.pone.0020071
                3098283
                21625517
                6ad49f7e-5e42-4d5a-9f55-4058c053fe45
                Bettus et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
                History
                : 18 October 2010
                : 25 April 2011
                Page count
                Pages: 11
                Categories
                Research Article
                Biology
                Neuroscience
                Neuroanatomy
                Connectomics
                Neuroimaging
                Fmri
                Medicine
                Anatomy and Physiology
                Electrophysiology
                Neurology
                Epilepsy
                Temporal Lobe Epilepsy

                Uncategorized
                Uncategorized

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