Epileptic Discharges Affect the Default Mode Network – fMRI and Intracerebral EEG Evidence

Functional neuroimaging studies of epilepsy patients often show, at the time of epileptic activity, deactivation in default mode network (DMN) regions, which is hypothesized to reflect altered consciousness. We aimed to study the metabolic and electrophysiological correlates of these changes in the DMN regions. We studied six epilepsy patients that underwent scalp EEG-fMRI and later stereotaxic intracerebral EEG (SEEG) sampling regions of DMN (posterior cingulate cortex, Pre-cuneus, inferior parietal lobule, medial prefrontal cortex and dorsolateral frontal cortex) as well as non-DMN regions. SEEG recordings were subject to frequency analyses comparing sections with interictal epileptic discharges (IED) to IED-free baselines in the IED-generating region, DMN and non-DMN regions. EEG-fMRI and SEEG were obtained at rest. During IEDs, EEG-fMRI demonstrated deactivation in various DMN nodes in 5 of 6 patients, most frequently the pre-cuneus and inferior parietal lobule, and less frequently the other DMN nodes. SEEG analyses demonstrated decrease in gamma power (50–150 Hz), and increase in the power of lower frequencies (<30 Hz) at times of IEDs, in at least one DMN node in all patients. These changes were not apparent in the non-DMN regions. We demonstrate that, at the time of IEDs, DMN regions decrease their metabolic demand and undergo an EEG change consisting of decreased gamma and increased lower frequencies. These findings, specific to DMN regions, confirm in a pathological condition a direct relationship between DMN BOLD activity and EEG activity. They indicate that epileptic activity affects the DMN, and therefore may momentarily reduce the consciousness level and cognitive reserve.

[1]  Robert Turner,et al.  A Method for Removing Imaging Artifact from Continuous EEG Recorded during Functional MRI , 2000, NeuroImage.

[2]  John C. Gore,et al.  Cluster analysis detection of functional MRI activity in temporal lobe epilepsy , 2007, Epilepsy Research.

[3]  R. Buckner,et al.  Functional-Anatomic Fractionation of the Brain's Default Network , 2010, Neuron.

[4]  Pierre LeVan,et al.  High‐Frequency Intracerebral EEG Activity (100–500 Hz) Following Interictal Spikes , 2006, Epilepsia.

[5]  Li Yang,et al.  Impaired consciousness in temporal lobe seizures: role of cortical slow activity. , 2010, Brain : a journal of neurology.

[6]  J. Maunsell,et al.  Different Origins of Gamma Rhythm and High-Gamma Activity in Macaque Visual Cortex , 2011, PLoS biology.

[7]  I. Fried,et al.  Coupling between Neuronal Firing Rate, Gamma LFP, and BOLD fMRI Is Related to Interneuronal Correlations , 2007, Current Biology.

[8]  Philippe Kahane,et al.  Exploring the electrophysiological correlates of the default ‐ mode network with intracerebral EEG , 2022 .

[9]  E. Martin,et al.  Simultaneous EEG-fMRI during a Working Memory Task: Modulations in Low and High Frequency Bands , 2010, PloS one.

[10]  Juan R. Vidal,et al.  Transient Suppression of Broadband Gamma Power in the Default-Mode Network Is Correlated with Task Complexity and Subject Performance , 2011, The Journal of Neuroscience.

[11]  Francesca Benuzzi,et al.  Increased cortical BOLD signal anticipates generalized spike and wave discharges in adolescents and adults with idiopathic generalized epilepsies , 2012, Epilepsia.

[12]  K. Miller,et al.  Direct electrophysiological measurement of human default network areas , 2009, Proceedings of the National Academy of Sciences.

[13]  M. Fukunaga,et al.  Low frequency BOLD fluctuations during resting wakefulness and light sleep: A simultaneous EEG‐fMRI study , 2008, Human brain mapping.

[14]  J. Gotman,et al.  EEG-fMRI , 2009, Neurology.

[15]  Mohamad Z. Koubeissi,et al.  Analysis of dynamics and propagation of parietal cingulate seizures with secondary mesial temporal involvement , 2009, Epilepsy & Behavior.

[16]  Yuan Zhou,et al.  Functional dysconnectivity of the dorsolateral prefrontal cortex in first-episode schizophrenia using resting-state fMRI , 2007, Neuroscience Letters.

[17]  Jean Gotman,et al.  Widespread epileptic networks in focal epilepsies: EEG‐fMRI study , 2012, Epilepsia.

[18]  J. Gotman,et al.  Quality of EEG in simultaneous EEG-fMRI for epilepsy , 2003, Clinical Neurophysiology.

[19]  Alan C. Evans,et al.  A General Statistical Analysis for fMRI Data , 2000, NeuroImage.

[20]  M. Greicius,et al.  Default-mode network activity distinguishes Alzheimer's disease from healthy aging: Evidence from functional MRI , 2004, Proc. Natl. Acad. Sci. USA.

[21]  Michael D. Greicius,et al.  Development of functional and structural connectivity within the default mode network in young children , 2010, NeuroImage.

[22]  M. Raichle,et al.  Cortical network functional connectivity in the descent to sleep , 2009, Proceedings of the National Academy of Sciences.

[23]  Joshua E. Motelow,et al.  Cortical and subcortical networks in human secondarily generalized tonic-clonic seizures. , 2009, Brain : a journal of neurology.

[24]  Colin Studholme,et al.  Positive and negative network correlations in temporal lobe epilepsy. , 2004, Cerebral cortex.

[25]  R. Schmidt,et al.  Cross-Frequency Phase–Phase Coupling between Theta and Gamma Oscillations in the Hippocampus , 2012, The Journal of Neuroscience.

[26]  Jean Gotman,et al.  EEG‐fMRI of focal epileptic spikes: Analysis with multiple haemodynamic functions and comparison with gadolinium‐enhanced MR angiograms , 2004, Human brain mapping.

[27]  J. Gotman,et al.  Generalized epileptic discharges show thalamocortical activation and suspension of the default state of the brain. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[28]  O. Dietrich,et al.  Test–retest reproducibility of the default‐mode network in healthy individuals , 2009, Human brain mapping.

[29]  G L Shulman,et al.  INAUGURAL ARTICLE by a Recently Elected Academy Member:A default mode of brain function , 2001 .

[30]  K. Meador,et al.  Pathophysiology of altered consciousness during seizures: Subtraction SPECT study , 2002, Neurology.

[31]  O. Bertrand,et al.  Relationship between task‐related gamma oscillations and BOLD signal: New insights from combined fMRI and intracranial EEG , 2007, Human brain mapping.

[32]  Jean Gotman,et al.  Erratum: High-frequency intracerebral EEG activity (100-500 Hz) following interictal spikes (Epilepsia (2006) 47, (1465-1476)) , 2006 .

[33]  Jean Gotman,et al.  Interictal high-frequency oscillations (100-500 Hz) in the intracerebral EEG of epileptic patients. , 2007, Brain : a journal of neurology.

[34]  Hal Blumenfeld,et al.  Why do Seizures Cause Loss of Consciousness? , 2003, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[35]  D. Spencer,et al.  Ictal neocortical slowing in temporal lobe epilepsy , 2004, Neurology.

[36]  Timothy M. Ellmore,et al.  Frequency-specific electrocorticographic correlates of working memory delay period fMRI activity , 2011, NeuroImage.

[37]  N. Logothetis,et al.  Neurophysiological investigation of the basis of the fMRI signal , 2001, Nature.

[38]  Jean Gotman,et al.  Structures involved at the time of temporal lobe spikes revealed by interindividual group analysis of EEG/fMRI data , 2009, Epilepsia.

[39]  Dennis L Barbour,et al.  Nonuniform High-Gamma (60–500 Hz) Power Changes Dissociate Cognitive Task and Anatomy in Human Cortex , 2011, The Journal of Neuroscience.

[40]  J. Gotman,et al.  Effect of sleep stage on interictal high‐frequency oscillations recorded from depth macroelectrodes in patients with focal epilepsy , 2009, Epilepsia.

[41]  Hal Blumenfeld,et al.  The role of subcortical structures in human epilepsy , 2002, Epilepsy & Behavior.

[42]  M. Corbetta,et al.  Electrophysiological signatures of resting state networks in the human brain , 2007, Proceedings of the National Academy of Sciences.

[43]  I. Fried,et al.  Coupling Between Neuronal Firing, Field Potentials, and fMRI in Human Auditory Cortex , 2005, Science.

[44]  Y. Benjamini,et al.  Controlling the false discovery rate: a practical and powerful approach to multiple testing , 1995 .

[45]  G. Glover,et al.  Resting-State Functional Connectivity in Major Depression: Abnormally Increased Contributions from Subgenual Cingulate Cortex and Thalamus , 2007, Biological Psychiatry.

[46]  A. Kleinschmidt,et al.  Temporal lobe interictal epileptic discharges affect cerebral activity in “default mode” brain regions , 2006, Human brain mapping.

[47]  I. Germano,et al.  Frameless stereotaxy for surgery of the epilepsies: preliminary experience. Technical note. , 1994, Journal of neurosurgery.