Ictal onset patterns of local field potentials, high frequency oscillations, and unit activity in human mesial temporal lobe epilepsy

Shennan Aibel Weiss*, Catalina Alvarado-Rojas, Anatol Bragin, Eric Behnke, Tony Fields, Itzhak Fried, Jerome Engel, Richard Staba

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

Abstract

Summary Objective To characterize local field potentials, high frequency oscillations, and single unit firing patterns in microelectrode recordings of human limbic onset seizures. Methods Wide bandwidth local field potential recordings were acquired from microelectrodes implanted in mesial temporal structures during spontaneous seizures from six patients with mesial temporal lobe epilepsy. Results In the seizure onset zone, distinct epileptiform discharges were evident in the local field potential prior to the time of seizure onset in the intracranial EEG. In all three seizures with hypersynchronous (HYP) seizure onset, fast ripples with incrementally increasing power accompanied epileptiform discharges during the transition to the ictal state (p < 0.01). In a single low voltage fast (LVF) onset seizure a triad of evolving HYP LFP discharges, increased single unit activity, and fast ripples of incrementally increasing power were identified ~20 s prior to seizure onset (p < 0.01). In addition, incrementally increasing fast ripples occurred after seizure onset just prior to the transition to LVF activity (p < 0.01). HYP onset was associated with an increase in fast ripple and ripple rate (p < 0.05) and commonly each HYP discharge had a superimposed ripple followed by a fast ripple. Putative excitatory and inhibitory single units could be distinguished during limbic seizure onset, and heterogeneous shifts in firing rate were observed during LVF activity. Significance Epileptiform activity is detected by microelectrodes before it is detected by depth macroelectrodes, and the one clinically identified LVF ictal onset was a HYP onset at the local level. Patterns of incrementally increasing fast ripple power are consistent with observations in rats with experimental hippocampal epilepsy, suggesting that limbic seizures arise when small clusters of synchronously bursting neurons increase in size, coalesce, and reach a critical mass for propagation.

Original languageEnglish
Pages (from-to)111-121
Number of pages11
JournalEpilepsia
Volume57
Issue number1
DOIs
StatePublished - 1 Jan 2016
Externally publishedYes

Funding

FundersFunder number
National Institutes of Health
National Institute of Neurological Disorders and StrokeR01NS071048, NS002808, NS033221, R01NS065877, R37NS033310, P20NS080181

    Keywords

    • Fast ripple
    • High frequency oscillation
    • Hypersynchronous
    • Limbic seizure
    • Low voltage fast
    • Ripple

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