Epileptic discharges specifically affect intrinsic connectivity networks during absence seizures

Intrinsic connectivity network (ICN) technique provides a feasible way for evaluating cognitive impairments in epilepsy. This EEG-fMRI study aims to comprehensively assess the alterations of ICNs affected by generalized spike-and-wave discharge (GSWD) during absence seizure (AS). Twelve fMRI sessions with GSWD, and individually paired non-GSWD sessions were acquired from 16 patients with AS. Ten ICNs corresponding to seizure origination and cognitive processes were extracted using independent component analysis. Intra- and inter-network connectivity alterations of the ICNs were observed through comparisons between GSWD and non-GSWD sessions. Sequential correlation analysis between GSWD and the ICN time courses addressed the immediate effects of GSWD on ICNs during AS. GSWD-related increase of intra-network connectivity was found only in the thalamus, and extensive decreases were found in the ICNs corresponding to higher-order cognitive processes including the default-mode network, dorsal attention network, central executive network and salience network. The perceptive networks and motor network were less affected by GSWD. Sequential correlation analysis further demonstrated different responses of the ICNs to GSWD. In addition to GSWD-related functional excitation in the thalamus and functional suspension in the default-mode network, this study revealed extensive inhibitions in the other ICNs corresponding to higher-order cognitive processes, and spared perceptive and motor processes in AS. GSWD elevated synchronization of brain network activity and sequentially affected the ICNs.

[1]  S Laureys,et al.  Intrinsic Brain Activity in Altered States of Consciousness , 2008, Annals of the New York Academy of Sciences.

[2]  H. Blumenfeld.  Impaired consciousness in epilepsy , 2012, The Lancet Neurology.

[3]  Q. Gong,et al.  Resting state basal ganglia network in idiopathic generalized epilepsy , 2012, Human brain mapping.

[4]  Jean Gotman,et al.  Functional connectivity in patients with idiopathic generalized epilepsy , 2011, Epilepsia.

[5]  S. Rombouts,et al.  Consistent resting-state networks across healthy subjects , 2006, Proceedings of the National Academy of Sciences.

[6]  M. Fox,et al.  Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging , 2007, Nature Reviews Neuroscience.

[7]  Jean Gotman,et al.  Independent component analysis reveals dynamic ictal BOLD responses in EEG-fMRI data from focal epilepsy patients , 2010, NeuroImage.

[8]  Hal Blumenfeld,et al.  Epilepsy and the consciousness system: transient vegetative state? , 2011, Neurologic clinics.

[9]  W. Liao,et al.  Impaired attention network in temporal lobe epilepsy: A resting FMRI study , 2009, Neuroscience Letters.

[10]  Wei Zhang,et al.  Selective aberrant functional connectivity of resting state networks in social anxiety disorder , 2010, NeuroImage.

[11]  Walter H Backes,et al.  Functional MRI in chronic epilepsy: associations with cognitive impairment , 2010, The Lancet Neurology.

[12]  Matthew N. DeSalvo,et al.  Dynamic Time Course of Typical Childhood Absence Seizures: EEG, Behavior, and Functional Magnetic Resonance Imaging , 2010, The Journal of Neuroscience.

[13]  J. Gotman,et al.  Absence seizures: Individual patterns revealed by EEG‐fMRI , 2010, Epilepsia.

[14]  Hal Blumenfeld,et al.  Impaired attention and network connectivity in childhood absence epilepsy , 2011, NeuroImage.

[15]  Wei Liao,et al.  Altered resting state networks in epileptic patients with generalized tonic–clonic seizures , 2011, Brain Research.

[16]  John S. Duncan,et al.  Independent component analysis of interictal fMRI in focal epilepsy: Comparison with general linear model-based EEG-correlated fMRI , 2007, NeuroImage.

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

[18]  Eswar Damaraju,et al.  Tracking whole-brain connectivity dynamics in the resting state. , 2014, Cerebral cortex.

[19]  M. Boly,et al.  Default network connectivity reflects the level of consciousness in non-communicative brain-damaged patients. , 2010, Brain : a journal of neurology.

[20]  Karl J. Friston,et al.  Functional magnetic resonance imaging of human absence seizures , 2003, Annals of neurology.

[21]  O. Snead,et al.  Basic mechanisms of generalized absence seizures , 1995, Annals of neurology.

[22]  Cheng Luo,et al.  EEG–fMRI study on the interictal and ictal generalized spike-wave discharges in patients with childhood absence epilepsy , 2009, Epilepsy Research.

[23]  J. Arends,et al.  The Relative Influence of Epileptic EEG Discharges, Short Nonconvulsive Seizures, and Type of Epilepsy on Cognitive Function , 2004, Epilepsia.

[24]  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.

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

[26]  M. Raichle,et al.  Disease and the brain's dark energy , 2010, Nature Reviews Neurology.

[27]  Andrei G. Vlassenko,et al.  Regulation of blood flow in activated human brain by cytosolic NADH/NAD+ ratio. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[28]  I. Scheffer,et al.  The core network in absence epilepsy , 2010, Neurology.

[29]  Tülay Adali,et al.  Estimating the number of independent components for functional magnetic resonance imaging data , 2007, Human brain mapping.

[30]  V. Calhoun,et al.  Aberrant localization of synchronous hemodynamic activity in auditory cortex reliably characterizes schizophrenia , 2004, Biological Psychiatry.

[31]  Jerome Engel,et al.  A Proposed Diagnostic Scheme for People with Epileptic Seizures and with Epilepsy: Report of the ILAE Task Force on Classification and Terminology , 2001, Epilepsia.

[32]  H. Siebner,et al.  Simultaneous EEG‐fMRI in drug‐naive children with newly diagnosed absence epilepsy , 2008, Epilepsia.

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

[34]  Hal Blumenfeld,et al.  Simultaneous EEG, fMRI, and behavior in typical childhood absence seizures , 2010, Epilepsia.

[35]  Q. Gong,et al.  Altered functional connectivity in default mode network in absence epilepsy: A resting‐state fMRI study , 2011, Human brain mapping.

[36]  M. Greicius,et al.  Persistent default‐mode network connectivity during light sedation , 2008, Human brain mapping.

[37]  F. H. Lopes da Silva,et al.  Evolving concepts on the pathophysiology of absence seizures: the cortical focus theory. , 2005, Archives of neurology.

[38]  Maurizio Corbetta,et al.  Large-scale brain networks account for sustained and transient activity during target detection , 2009, NeuroImage.

[39]  G. Glover,et al.  Dissociable Intrinsic Connectivity Networks for Salience Processing and Executive Control , 2007, The Journal of Neuroscience.

[40]  Cheng Luo,et al.  Altered resting‐state connectivity during interictal generalized spike‐wave discharges in drug‐naïve childhood absence epilepsy , 2013, Human brain mapping.