High-frequency oscillations in epileptic brain

Purpose of reviewIt has been 10 years since pathological high-frequency oscillations (pHFOs) were described in the brain of epileptic animals and patients. This review summarizes progress in research on mechanisms of their generation and potential clinical applications over that period. Recent findingsInitially, pHFOs were recorded with microelectrodes in the hippocampus of rodents and patients with mesial temporal lobe epilepsy (MTLE), but recently pHFOs have also been recorded with clinical depth and grid electrodes in multiple brain areas including the hippocampus and neocortex of patients with different types of epilepsy. One hypothesis is that pHFOs reflect fields of hypersynchronized action potentials (bursts of population spikes) within small discrete neuronal clusters responsible for seizure generation. Studies suggest that pHFOs can be used as a reliable biomarker for epileptogenesis, epileptogenicity, and the delineation of the epileptogenic region. SummaryRecording of pHFOs with clinical electrodes provides a means for further investigation of their functional role in the epileptic brain and as a potential biomarker of epileptogenesis and epileptogenicity and for presurgical mapping.

[1]  Ayako Ochi,et al.  Topographic Movie of Ictal High‐Frequency Oscillations on the Brain Surface Using Subdural EEG in Neocortical Epilepsy , 2006, Epilepsia.

[2]  Caterina Giannini,et al.  Phase I trial: safety and feasibility of intracranial electroencephalography using hybrid subdural electrodes containing macro- and microelectrode arrays. , 2008, Neurosurgical focus.

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

[5]  G Curio,et al.  Localization of evoked neuromagnetic 600 Hz activity in the cerebral somatosensory system. , 1994, Electroencephalography and clinical neurophysiology.

[6]  M. Low,et al.  Questions regarding the sequential neural generator theory of the somatosensory evoked potential raised by digital filtering. , 1984, Electroencephalography and clinical neurophysiology.

[7]  G Buzsáki,et al.  Cellular–Synaptic Generation of Sleep Spindles, Spike-and-Wave Discharges, and Evoked Thalamocortical Responses in the Neocortex of the Rat , 1997, The Journal of Neuroscience.

[8]  G. Buzsáki,et al.  tFast Network Oscillations in the Hippocampal CA1 Region of the Behaving Rat , 1999, The Journal of Neuroscience.

[9]  M. Wilson,et al.  Coordinated Interactions between Hippocampal Ripples and Cortical Spindles during Slow-Wave Sleep , 1998, Neuron.

[10]  Comparison of somatosensory evoked high-frequency oscillations after posterior tibial and median nerve stimulation , 1999, Clinical Neurophysiology.

[11]  Jean Gotman,et al.  Detection of changes of high-frequency activity by statistical time-frequency analysis in epileptic spikes , 2009, Clinical Neurophysiology.

[12]  Ayako Ochi,et al.  Epileptic spasms in older pediatric patients: MEG and ictal high-frequency oscillations suggest focal-onset seizures in a subset of epileptic spasms , 2008, Epilepsy Research.

[13]  R. Cracco,et al.  Somatosensory evoked potential in man: far field potentials. , 1976, Electroencephalography and clinical neurophysiology.

[14]  Jerome Engel,et al.  Voltage Depth Profiles of High‐frequency Oscillations after Kainic Acid‐induced Status Epilepticus , 2007, Epilepsia.

[15]  J. Born,et al.  Temporal coupling of parahippocampal ripples, sleep spindles and slow oscillations in humans. , 2007, Brain : a journal of neurology.

[16]  N. Ulanovsky,et al.  Hippocampal cellular and network activity in freely moving echolocating bats , 2007, Nature Neuroscience.

[17]  Ayako Ochi,et al.  Focal cortical high-frequency oscillations trigger epileptic spasms: Confirmation by digital video subdural EEG , 2005, Clinical Neurophysiology.

[18]  Charles L. Wilson,et al.  Analysis of Chronic Seizure Onsets after Intrahippocampal Kainic Acid Injection in Freely Moving Rats , 2005, Epilepsia.

[19]  M. Curtis,et al.  Interictal spikes in focal epileptogenesis , 2001, Progress in Neurobiology.

[20]  G. Buzsáki,et al.  High-Frequency Oscillations in the Output Networks of the Hippocampal–Entorhinal Axis of the Freely Behaving Rat , 1996, The Journal of Neuroscience.

[21]  J. Gotman,et al.  High frequency oscillations (80–500 Hz) in the preictal period in patients with focal seizures , 2009, Epilepsia.

[22]  D. Barth,et al.  Submillisecond Synchronization of Fast Electrical Oscillations in Neocortex , 2003, The Journal of Neuroscience.

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

[24]  Charles L. Wilson,et al.  High‐frequency oscillations recorded in human medial temporal lobe during sleep , 2004, Annals of neurology.

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

[26]  A. Bragin,et al.  Spatial Stability over Time of Brain Areas Generating Fast Ripples in the Epileptic Rat , 2003, Epilepsia.

[27]  Jean Gotman,et al.  High frequency oscillations and seizure frequency in patients with focal epilepsy , 2009, Epilepsy Research.

[28]  J. Martinerie,et al.  Mapping interictal oscillations greater than 200 Hz recorded with intracranial macroelectrodes in human epilepsy. , 2010, Brain : a journal of neurology.

[29]  J. O’Keefe.  Place units in the hippocampus of the freely moving rat , 1976, Experimental Neurology.

[30]  Eileen Luders,et al.  Three‐dimensional surface maps link local atrophy and fast ripples in human epileptic hippocampus , 2009, Annals of neurology.

[31]  B. Litt,et al.  High-frequency oscillations in human temporal lobe: simultaneous microwire and clinical macroelectrode recordings. , 2008, Brain : a journal of neurology.

[32]  C. Schroeder,et al.  Spatial characterization of interictal high frequency oscillations in epileptic neocortex , 2009, Brain : a journal of neurology.

[33]  J. Gotman,et al.  High frequency oscillations in intracranial EEGs mark epileptogenicity rather than lesion type. , 2009, Brain : a journal of neurology.

[34]  C. Wilson,et al.  Electrophysiologic Analysis of a Chronic Seizure Model After Unilateral Hippocampal KA Injection , 1999, Epilepsia.

[35]  J Gotman,et al.  High-frequency oscillations mirror disease activity in patients with epilepsy , 2009, Neurology.

[36]  Jeffery A. Hall,et al.  Interictal high‐frequency oscillations (80–500 Hz) are an indicator of seizure onset areas independent of spikes in the human epileptic brain , 2008, Epilepsia.

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

[38]  Ayako Ochi,et al.  Dynamic Changes of Ictal High‐Frequency Oscillations in Neocortical Epilepsy: Using Multiple Band Frequency Analysis , 2007, Epilepsia.

[39]  A. Bragin,et al.  Chronic Epileptogenesis Requires Development of a Network of Pathologically Interconnected Neuron Clusters: A Hypothesis , 2000, Epilepsia.

[40]  M. Steriade,et al.  Neocortical very fast oscillations (ripples, 80-200 Hz) during seizures: intracellular correlates. , 2003, Journal of neurophysiology.

[41]  Charles L. Wilson,et al.  Local Generation of Fast Ripples in Epileptic Brain , 2002, The Journal of Neuroscience.

[42]  Itzhak Fried,et al.  Interictal high‐frequency oscillations (80–500Hz) in the human epileptic brain: Entorhinal cortex , 2002, Annals of neurology.

[43]  G Buzsáki,et al.  The hippocampo-neocortical dialogue. , 1996, Cerebral cortex.

[44]  Jean Gotman,et al.  Value of electrical stimulation and high frequency oscillations (80–500 Hz) in identifying epileptogenic areas during intracranial EEG recordings , 2010, Epilepsia.

[45]  J. Fell,et al.  Ripples in the medial temporal lobe are relevant for human memory consolidation. , 2008, Brain : a journal of neurology.

[46]  Charles L. Wilson,et al.  High‐frequency Oscillations after Status Epilepticus: Epileptogenesis and Seizure Genesis , 2004, Epilepsia.

[47]  G. K. Smith,et al.  Spontaneous EEG spikes in the normal hippocampus. II. Relations to synchronous burst discharges. , 1988, Electroencephalography and clinical neurophysiology.

[48]  Jean Gotman,et al.  Improving the identification of High Frequency Oscillations , 2009, Clinical Neurophysiology.

[49]  D. Barth,et al.  Spatiotemporal organization of fast (>200 Hz) electrical oscillations in rat Vibrissa/Barrel cortex. , 1999, Journal of neurophysiology.

[50]  B. Litt,et al.  High-frequency oscillations and seizure generation in neocortical epilepsy. , 2004, Brain : a journal of neurology.

[51]  Brian Litt,et al.  Human and automated detection of high-frequency oscillations in clinical intracranial EEG recordings , 2007, Clinical Neurophysiology.

[52]  Houman Khosravani,et al.  Spatial localization and time‐dependant changes of electrographic high frequency oscillations in human temporal lobe epilepsy , 2009, Epilepsia.

[53]  Helen J. Cross,et al.  A Possible Role for Gap Junctions in Generation of Very Fast EEG Oscillations Preceding the Onset of, and Perhaps Initiating, Seizures , 2001, Epilepsia.

[54]  G. Buzsáki,et al.  Sharp wave-associated high-frequency oscillation (200 Hz) in the intact hippocampus: network and intracellular mechanisms , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[55]  Kenneth D Harris,et al.  Selective Impairment of Hippocampal Gamma Oscillations in Connexin-36 Knock-Out Mouse In Vivo , 2003, The Journal of Neuroscience.

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

[57]  Itzhak Fried,et al.  Increased Fast ripple to ripple Ratios Correlate with Reduced Hippocampal Volumes and Neuron Loss in Temporal Lobe Epilepsy Patients , 2007, Epilepsia.

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

[59]  P J Allen,et al.  Very high-frequency rhythmic activity during SEEG suppression in frontal lobe epilepsy. , 1991, Electroencephalography and clinical neurophysiology.

[60]  Charles L. Wilson,et al.  Cell Type-Specific Firing during Ripple Oscillations in the Hippocampal Formation of Humans , 2008, The Journal of Neuroscience.

[61]  Chris I. De Zeeuw,et al.  GATA-3 Is Involved in the Development of Serotonergic Neurons in the Caudal Raphe Nuclei , 1999, The Journal of Neuroscience.

[62]  I. Módy,et al.  High‐frequency oscillations: What is normal and what is not? , 2009, Epilepsia.

[63]  F. Dudek,et al.  Intracellular correlates of fast (>200 Hz) electrical oscillations in rat somatosensory cortex. , 2000, Journal of neurophysiology.

[64]  Charles L. Wilson,et al.  Quantitative analysis of high-frequency oscillations (80-500 Hz) recorded in human epileptic hippocampus and entorhinal cortex. , 2002, Journal of neurophysiology.

[65]  Charles L. Wilson,et al.  Hippocampal and Entorhinal Cortex High‐Frequency Oscillations (100–500 Hz) in Human Epileptic Brain and in Kainic Acid‐Treated Rats with Chronic Seizures , 1999, Epilepsia.

[66]  G. Buzsáki,et al.  High-frequency network oscillation in the hippocampus. , 1992, Science.