Neuronal Firing and Waveform Alterations through Ictal Recruitment in Humans
| Autor: | Sameer A. Sheth, Paul A. House, Lisa M. Bateman, Robert R. Goodman, Andrew J. Trevelyan, Ronald G. Emerson, Guy M. McKhann, Bradley Greger, Edward M. Merricks, Catherine A. Schevon, Elliot H. Smith |
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| Rok vydání: | 2020 |
| Předmět: |
Adult
Male Recruitment Neurophysiological 0301 basic medicine Drug Resistant Epilepsy Neuronal firing Wavelet Analysis Action Potentials Biology Young Adult 03 medical and health sciences Epilepsy 0302 clinical medicine Seizures medicine Humans Waveform Premovement neuronal activity Ictal Research Articles 030304 developmental biology Cerebral Cortex Neurons 0303 health sciences General Neuroscience Electroencephalography Multielectrode array Middle Aged medicine.disease Brain Waves Cortex (botany) 030104 developmental biology nervous system Spike sorting Ionic conductance Female Tonic firing Animal studies Neuroscience 030217 neurology & neurosurgery |
| Zdroj: | J Neurosci |
| ISSN: | 1529-2401 0270-6474 |
| DOI: | 10.1523/jneurosci.0417-20.2020 |
| Popis: | Clinical analyses of neuronal activity during seizures, invariably using extracellular recordings, is greatly hindered by various phenomena that are well established in animal studies: changes in local ionic concentration, changes in ionic conductance, and intense, hypersynchronous firing. The first two alter the action potential waveform, whereas the third increases the “noise”; all three factors confound attempts to detect and classify single neurons (units). To address these analytical difficulties, we developed a novel template-matching based spike sorting method, which enabled identification of 1,239 single units in 27 patients with intractable focal epilepsy, that were tracked throughout multiple seizures. These new analyses showed continued neuronal firing through the ictal transition, which was defined as a transient period of intense tonic firing consistent with previous descriptions of the ictal wavefront. After the ictal transition, neurons displayed increased spike duration (p < 0.001) and reduced spike amplitude (p < 0.001), in keeping with prior animal studies; units in non-recruited territories, by contrast, showed more stable waveforms. All units returned to their pre-ictal waveforms after seizure termination. Waveshape changes were stereotyped across seizures within patients. Our analyses of single neuron firing patterns, at the ictal wavefront, showed widespread intense activation, and commonly involving marked waveshape alteration. We conclude that the distinction between tissue that has been recruited to the seizure versus non-recruited territories is evident at the level of single neurons, and that increased waveform duration and decreased waveform amplitude are hallmarks of seizure invasion that could be used as defining characteristics of local recruitment.Significance StatementAnimal studies consistently show marked changes in action potential waveform during epileptic discharges, but acquiring similar evidence in humans has proved difficult. Assessing neuronal involvement in ictal events is pivotal to understanding seizure dynamics and in defining clinical localization of epileptic pathology. Using a novel method to track neuronal firing, we analyzed microelectrode array recordings of spontaneously occurring human seizures, and here report two dichotomous activity patterns. In cortex that is recruited to the seizure, neuronal firing rates increase and waveforms become longer in duration and shorter in amplitude, while penumbral tissue shows stable action potentials, in keeping with the “dual territory” model of seizure dynamics. |
| Databáze: | OpenAIRE |
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