Two Seizure-Onset Types Reveal Specific Patterns of High-Frequency Oscillations in a Model of Temporal Lobe Epilepsy

High-frequency oscillations (HFOs; 80–500 Hz) are thought to mirror the pathophysiological changes occurring in epileptic brains. However, the distribution of HFOs during seizures remains undefined. Here, we recorded from the hippocampal CA3 subfield, subiculum, entorhinal cortex, and dentate gyrus to quantify the occurrence of ripples (80–200 Hz) and fast ripples (250–500 Hz) during low-voltage fast-onset (LVF) and hypersynchronous-onset (HYP) seizures in the rat pilocarpine model of temporal lobe epilepsy. We discovered in LVF seizures that (1) progression from preictal to ictal activity was characterized in seizure-onset zones by an increase of ripple rates that were higher when compared with fast ripple rates and (2) ripple rates during the ictal period were higher compared with fast ripple rates in seizure-onset zones and later in regions of secondary spread. In contrast, we found in HYP seizures that (1) fast ripple rates increased during the preictal period and were higher compared with ripple rates in both seizure-onset zones and in regions of secondary spread and (2) they were still higher compared with ripple rates in both seizure-onset zones and regions of secondary spread during the ictal period. Our findings demonstrate that ripples and fast ripples show distinct time- and region-specific patterns during LVF and HYP seizures, thus suggesting that they play specific roles in ictogenesis.

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

[2]  M. Avoli,et al.  GABAergic synchronization in the limbic system and its role in the generation of epileptiform activity , 2011, Progress in Neurobiology.

[3]  M. Avoli,et al.  Participation of GABAA-mediated inhibition in ictallike discharges in the rat entorhinal cortex. , 1998, Journal of neurophysiology.

[4]  Fernando Lopes da Silva,et al.  High-frequency oscillations – Where we are and where we need to go , 2012, Progress in Neurobiology.

[5]  R. Miles,et al.  Glutamatergic pre-ictal discharges emerge at the transition to seizure in human epilepsy , 2011, Nature Neuroscience.

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

[7]  Jean Gotman,et al.  Ictal and interictal high frequency oscillations in patients with focal epilepsy , 2011, Clinical Neurophysiology.

[8]  C. Bénar,et al.  Pitfalls of high-pass filtering for detecting epileptic oscillations: A technical note on “false” ripples , 2010, Clinical Neurophysiology.

[9]  J. Kapur,et al.  A combination of ketamine and diazepam synergistically controls refractory status epilepticus induced by cholinergic stimulation , 2008, Epilepsia.

[10]  A. Murro,et al.  The significance of ictal depth EEG patterns in patients with temporal lobe epilepsy. , 1996, Electroencephalography and clinical neurophysiology.

[11]  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.

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

[13]  Jean Gotman,et al.  Convulsive status epilepticus duration as determinant for epileptogenesis and interictal discharge generation in the rat limbic system , 2010, Neurobiology of Disease.

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

[15]  Houman Khosravani,et al.  Increased High‐frequency Oscillations Precede in vitro Low‐Mg2+ Seizures , 2005, Epilepsia.

[16]  J. Gotman,et al.  High‐frequency electroencephalographic oscillations correlate with outcome of epilepsy surgery , 2010, Annals of neurology.

[17]  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.

[18]  Gabriella Panuccio,et al.  On the ictogenic properties of the piriform cortex in vitro , 2012, Epilepsia.

[19]  Kevin J. Staley,et al.  Mechanisms of Fast Ripples in the Hippocampus , 2004, The Journal of Neuroscience.

[20]  Guglielmo Foffani,et al.  Emergent Dynamics of Fast Ripples in the Epileptic Hippocampus , 2010, The Journal of Neuroscience.

[21]  Charles L. Wilson,et al.  Functional and Anatomic Correlates of Two Frequently Observed Temporal Lobe Seizure-Onset Patterns , 2000, Neural plasticity.

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

[23]  Guglielmo Foffani,et al.  Reduced Spike-Timing Reliability Correlates with the Emergence of Fast Ripples in the Rat Epileptic Hippocampus , 2007, Neuron.

[24]  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.

[25]  R. Racine,et al.  Modification of seizure activity by electrical stimulation. II. Motor seizure. , 1972, Electroencephalography and clinical neurophysiology.

[26]  G. Mathern,et al.  Removing interictal fast ripples on electrocorticography linked with seizure freedom in children , 2010, Neurology.

[27]  Alejandro F. Bujan,et al.  High-Frequency Network Activity, Global Increase in Neuronal Activity, and Synchrony Expansion Precede Epileptic Seizures In Vitro , 2010, The Journal of Neuroscience.

[28]  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.

[29]  Jerome Engel,et al.  The Cause of the Imbalance in the Neuronal Network Leading to Seizure Activity Can Be Predicted by the Electrographic Pattern of the Seizure Onset , 2009, The Journal of Neuroscience.

[30]  John G. R. Jefferys,et al.  Epileptic high-frequency network activity in a model of non-lesional temporal lobe epilepsy , 2010, Brain : a journal of neurology.

[31]  Fiona E. N. LeBeau,et al.  A Possible Role for Gap Junctions in Generation of Very Fast EEG Oscillations Preceding the Onset of, and Perhaps Initiating, Seizures , 2001 .

[32]  Farshad Kheiri,et al.  Further evidence that pathologic high‐frequency oscillations are bursts of population spikes derived from recordings of identified cells in dentate gyrus , 2011, Epilepsia.

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

[34]  Jean Gotman,et al.  Contact size does not affect high frequency oscillation detection in intracerebral EEG recordings in a rat epilepsy model , 2011, Clinical Neurophysiology.

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

[36]  M. Avoli,et al.  Laminar organization of epileptiform discharges in the rat entorhinal cortex in vitro , 1998, The Journal of physiology.

[37]  I. Módy,et al.  High-frequency oscillations : What is normal and what is not ? , 2008 .

[38]  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.

[39]  L. Swanson.  The Rat Brain in Stereotaxic Coordinates, George Paxinos, Charles Watson (Eds.). Academic Press, San Diego, CA (1982), vii + 153, $35.00, ISBN: 0 125 47620 5 , 1984 .

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

[41]  Fabrice Wendling,et al.  Mechanisms of physiological and epileptic HFO generation , 2012, Progress in Neurobiology.

[42]  Jean Gotman,et al.  High-frequency (80–500Hz) oscillations and epileptogenesis in temporal lobe epilepsy , 2011, Neurobiology of Disease.

[43]  R. Racine,et al.  Modification of seizure activity by electrical stimulation. 3. Mechanisms. , 1972, Electroencephalography and clinical neurophysiology.