Epilepsy as a Disorder of Cortical Network Organization

The brain is naturally considered as a network of interacting elements which, when functioning properly, produces an enormous range of dynamic, adaptable behavior. However, when elements of this network fail, pathological changes ensue, including epilepsy, one of the most common brain disorders. This review examines some aspects of cortical network organization that distinguish epileptic cortex from normal brain as well as the dynamics of network activity before and during seizures, focusing primarily on focal seizures. The review is organized around four phases of the seizure: the interictal period, onset, propagation, and termination. For each phase, the authors discuss the most common rhythmic characteristics of macroscopic brain voltage activity and outline the observed functional network features. Although the characteristics of functional networks that support the epileptic seizure remain an area of active research, the prevailing trends point to a complex set of network dynamics between, before, and during seizures.

[1]  R.N.Dej.,et al.  Epilepsy and the Functional Anatomy of the Human Brain , 1954, Neurology.

[2]  S. Brenner,et al.  The structure of the nervous system of the nematode Caenorhabditis elegans. , 1986, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[3]  R. Fisher,et al.  High-frequency EEG activity at the start of seizures. , 1992, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[4]  Karl J. Friston Functional and effective connectivity in neuroimaging: A synthesis , 1994 .

[5]  G. Alarcón,et al.  Power spectrum and intracranial EEG patterns at seizure onset in partial epilepsy. , 1995, Electroencephalography and clinical neurophysiology.

[6]  György Buzsáki,et al.  Gamma frequency oscillation in the hippocampus of the rat: intracellular analysis in vivo , 1998, The European journal of neuroscience.

[7]  Duncan J. Watts,et al.  Collective dynamics of ‘small-world’ networks , 1998, Nature.

[8]  V L Towle,et al.  Electrocorticographic coherence patterns. , 1999, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[9]  P. Grassberger,et al.  A robust method for detecting interdependences: application to intracranially recorded EEG , 1999, chao-dyn/9907013.

[10]  Charles L. Wilson,et al.  High‐frequency oscillations in human brain , 1999, Hippocampus.

[11]  D. Colella,et al.  Brain chirps: spectrographic signatures of epileptic seizures , 2000, Clinical Neurophysiology.

[12]  F. Mormann,et al.  Mean phase coherence as a measure for phase synchronization and its application to the EEG of epilepsy patients , 2000 .

[13]  D. McCormick,et al.  On the cellular and network bases of epileptic seizures. , 2001, Annual review of physiology.

[14]  P. Mangan,et al.  The Midline Thalamus: Alterations and a Potential Role in Limbic Epilepsy , 2001, Epilepsia.

[15]  M. Steriade,et al.  Focal synchronization of ripples (80-200 Hz) in neocortex and their neuronal correlates. , 2001, Journal of neurophysiology.

[16]  S. Schiff,et al.  Decreased Neuronal Synchronization during Experimental Seizures , 2002, The Journal of Neuroscience.

[17]  F. A. Gibbs,et al.  Epilepsy: a paroxysmal cerebral dysrhythmia , 2002, Epilepsy & Behavior.

[18]  Cornelis J Stam,et al.  Seizure detection in the neonatal EEG with synchronization likelihood , 2003, Clinical Neurophysiology.

[19]  Igor Timofeev,et al.  Partial cortical deafferentation promotes development of paroxysmal activity. , 2003, Cerebral cortex.

[20]  J. Bellanger,et al.  Epileptic fast intracerebral EEG activity: evidence for spatial decorrelation at seizure onset. , 2003, Brain : a journal of neurology.

[21]  Mark E. J. Newman,et al.  The Structure and Function of Complex Networks , 2003, SIAM Rev..

[22]  M. Steriade,et al.  Neocortical seizures: initiation, development and cessation , 2004, Neuroscience.

[23]  F. Wendling,et al.  Temporal lobe epilepsy , 2019, Radiopaedia.org.

[24]  J. White,et al.  Epilepsy in Small-World Networks , 2004, The Journal of Neuroscience.

[25]  Cornelis J Stam,et al.  Different EEG frequency band synchronization during nocturnal frontal lobe seizures , 2004, Clinical Neurophysiology.

[26]  B. Connors,et al.  Initiation, Propagation, and Termination of Epileptiform Activity in Rodent Neocortex In Vitro Involve Distinct Mechanisms , 2005, The Journal of Neuroscience.

[27]  Steven J. Schiff,et al.  Neuronal spatiotemporal pattern discrimination: The dynamical evolution of seizures , 2005, NeuroImage.

[28]  A. Kraskov,et al.  On the predictability of epileptic seizures , 2005, Clinical Neurophysiology.

[29]  Bethany Percha,et al.  Transition from local to global phase synchrony in small world neural network and its possible implications for epilepsy. , 2005, Physical review. E, Statistical, nonlinear, and soft matter physics.

[30]  Rodrigo Quian Quiroga,et al.  Nonlinear multivariate analysis of neurophysiological signals , 2005, Progress in Neurobiology.

[31]  D. Nair,et al.  Epilepsy , 1977, Journal of Neurology.

[32]  J. Gotman,et al.  High-frequency oscillations during human focal seizures. , 2006, Brain : a journal of neurology.

[33]  John S Duncan,et al.  Adult epilepsy , 2006, The Lancet.

[34]  Xin-Ping Guan,et al.  Networking Property During Epileptic Seizure with Multi-channel EEG Recordings , 2006, ISNN.

[35]  Danielle Smith Bassett,et al.  Small-World Brain Networks , 2006, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[36]  Lotfi Senhadji,et al.  Quantitative evaluation of linear and nonlinear methods characterizing interdependencies between brain signals. , 2006, Physical review. E, Statistical, nonlinear, and soft matter physics.

[37]  Changsong Zhou,et al.  Hierarchical organization unveiled by functional connectivity in complex brain networks. , 2006, Physical review letters.

[38]  J. Régis,et al.  The role of corticothalamic coupling in human temporal lobe epilepsy. , 2006, Brain : a journal of neurology.

[39]  Kaspar Anton Schindler,et al.  Increasing synchronization may promote seizure termination: Evidence from status epilepticus , 2007, Clinical Neurophysiology.

[40]  Kaspar Anton Schindler,et al.  Assessing seizure dynamics by analysing the correlation structure of multichannel intracranial EEG. , 2006, Brain : a journal of neurology.

[41]  Cornelis J Stam,et al.  Graph theoretical analysis of complex networks in the brain , 2007, Nonlinear biomedical physics.

[42]  Olaf Sporns,et al.  Network structure of cerebral cortex shapes functional connectivity on multiple time scales , 2007, Proceedings of the National Academy of Sciences.

[43]  C. Stam,et al.  Small-world networks and epilepsy: Graph theoretical analysis of intracerebrally recorded mesial temporal lobe seizures , 2007, Clinical Neurophysiology.

[44]  Matthäus Staniek,et al.  Measuring Synchronization in the Epileptic Brain: a Comparison of Different Approaches , 2007, Int. J. Bifurc. Chaos.

[45]  L. Tsimring,et al.  Topological determinants of epileptogenesis in large-scale structural and functional models of the dentate gyrus derived from experimental data. , 2007, Journal of neurophysiology.

[46]  R. Goodman,et al.  Cortical abnormalities in epilepsy revealed by local EEG synchrony , 2007, NeuroImage.

[47]  Lester Melie-García,et al.  Characterizing brain anatomical connections using diffusion weighted MRI and graph theory , 2007, NeuroImage.

[48]  Oren Sagher,et al.  Mapping and assessment of epileptogenic foci using frequency-entropy templates. , 2007, Physical review. E, Statistical, nonlinear, and soft matter physics.

[49]  M. Kramer,et al.  Emergent network topology at seizure onset in humans , 2008, Epilepsy Research.

[50]  Klaus Lehnertz,et al.  Evolving functional network properties and synchronizability during human epileptic seizures. , 2008, Chaos.

[51]  J. Régis,et al.  Enhanced EEG functional connectivity in mesial temporal lobe epilepsy , 2008, Epilepsy Research.

[52]  J. Pastor,et al.  Synchronization Clusters of Interictal Activity in the Lateral Temporal Cortex of Epileptic Patients: Intraoperative Electrocorticographic Analysis , 2008, Epilepsia.

[53]  Antonina Starita,et al.  Detection of Signs of Brain Dysfunction in Epileptic Children by Recognition of Transient Changes in the Correlation of Seizure-Free EEG , 2008, Brain Topography.

[54]  R. Morgan,et al.  Nonrandom connectivity of the epileptic dentate gyrus predicts a major role for neuronal hubs in seizures , 2008, Proceedings of the National Academy of Sciences.

[55]  Olaf Sporns,et al.  Symbiotic relationship between brain structure and dynamics , 2009, BMC Neuroscience.

[56]  O. Sporns,et al.  Mapping the Structural Core of Human Cerebral Cortex , 2008, PLoS biology.

[57]  S. Moshé,et al.  How do seizures stop? , 2008, Epilepsia.

[58]  Pablo Moscato,et al.  Distinguishing childhood absence epilepsy patients from controls by the analysis of their background brain electrical activity , 2009, Journal of Neuroscience Methods.

[59]  Eric D. Kolaczyk,et al.  Statistical Analysis of Network Data , 2009 .

[60]  K. Lehnertz,et al.  Synchronization phenomena in human epileptic brain networks , 2009, Journal of Neuroscience Methods.

[61]  Eric D. Kolaczyk,et al.  Statistical Analysis of Network Data: Methods and Models , 2009 .

[62]  Uri T Eden,et al.  Network inference with confidence from multivariate time series. , 2009, Physical review. E, Statistical, nonlinear, and soft matter physics.

[63]  Victoria Booth,et al.  Interaction of Cellular and Network Mechanisms in Spatiotemporal Pattern Formation in Neuronal Networks , 2009, The Journal of Neuroscience.

[64]  M. de Curtis,et al.  Reevaluating the mechanisms of focal ictogenesis: The role of low‐voltage fast activity , 2009, Epilepsia.

[65]  W. Liao,et al.  Impaired perceptual networks in temporal lobe epilepsy revealed by resting fMRI , 2009, Journal of Neurology.

[66]  O. Sporns,et al.  Complex brain networks: graph theoretical analysis of structural and functional systems , 2009, Nature Reviews Neuroscience.

[67]  Alan C. Evans,et al.  Mapping anatomical connectivity patterns of human cerebral cortex using in vivo diffusion tensor imaging tractography. , 2009, Cerebral cortex.

[68]  Lucas Antiqueira,et al.  Estimating complex cortical networks via surface recordings—A critical note , 2010, NeuroImage.

[69]  O. Sporns Networks of the Brain , 2010 .

[70]  Andreas Daffertshofer,et al.  The relationship between structural and functional connectivity: Graph theoretical analysis of an EEG neural mass model , 2010, NeuroImage.

[71]  C. Stam,et al.  ‘Functional Connectivity’ Is a Sensitive Predictor of Epilepsy Diagnosis after the First Seizure , 2010, PloS one.

[72]  Bin He,et al.  Neocortical seizure foci localization by means of a directed transfer function method , 2010, Epilepsia.

[73]  Kaspar Anton Schindler,et al.  Peri-ictal correlation dynamics of high-frequency (80–200Hz) intracranial EEG , 2010, Epilepsy Research.

[74]  M. Kramer,et al.  Coalescence and Fragmentation of Cortical Networks during Focal Seizures , 2010, The Journal of Neuroscience.

[75]  Huafu Chen,et al.  Altered Functional Connectivity and Small-World in Mesial Temporal Lobe Epilepsy , 2010, PloS one.

[76]  Olaf Sporns,et al.  Complex network measures of brain connectivity: Uses and interpretations , 2010, NeuroImage.

[77]  Roger D. Traub,et al.  Cortical Oscillations in Health and Disease , 2010 .

[78]  K. Lehnertz,et al.  State dependent properties of epileptic brain networks: Comparative graph–theoretical analyses of simultaneously recorded EEG and MEG , 2010, Clinical Neurophysiology.

[79]  Klaus Lehnertz,et al.  From brain to earth and climate systems: Small-world interaction networks or not? , 2011, Chaos.

[80]  Wulfram Gerstner,et al.  Extraction of Network Topology From Multi-Electrode Recordings: Is there a Small-World Effect? , 2011, Front. Comput. Neurosci..

[81]  E. Halgren,et al.  Single-neuron dynamics in human focal epilepsy , 2011, Nature Neuroscience.

[82]  Bin He,et al.  Graph analysis of epileptogenic networks in human partial epilepsy , 2011, Epilepsia.