Neuronal ensemble synchrony during human focal seizures

Wilson Truccolo, Omar J. Ahmed, Matthew T. Harrison, Emad N. Eskandar, G. Rees Cosgrove, Joseph R. Madsen, Andrew S. Blum, N. Stevenson Potter, Leigh R. Hochberg, Sydney S. Cash

Research output: Contribution to journalArticle

65 Scopus citations

Abstract

Seizures are classically characterized as the expression of hypersynchronous neural activity, yet the true degree of synchrony in neuronal spiking (action potentials) during human seizures remains a fundamental question. We quantified the temporal precision of spike synchrony in ensembles of neocortical neurons during seizures in people with pharmacologically intractable epilepsy. Two seizure types were analyzed: those characterized by sustained gamma (~40-60 Hz) local field potential (LFP) oscillations or by spike-wave complexes (SWCs; ~3 Hz). Fine (<10 ms) temporal synchrony was rarely present during gamma-band seizures, where neuronal spiking remained highly irregular and asynchronous. In SWC seizures, phase locking of neuronal spiking to the SWC spike phase induced synchrony at a coarse 50-100 ms level. In addition, transient fine synchrony occurred primarily during the initial ~20 ms period of the SWC spike phase and varied across subjects and seizures. Sporadic coherence events between neuronal population spike counts and LFPs were observed during SWC seizures in high (~80 Hz) gamma-band and during high-frequency oscillations (~130 Hz). Maximum entropy models of the joint neuronal spiking probability, constrained only on single neurons' nonstationary coarse spiking rates and local network activation, explained most of the fine synchrony in both seizure types. Our findings indicate that fine neuronal ensemble synchrony occurs mostly during SWC, not gamma-band, seizures, and primarily during the initial phase of SWC spikes. Furthermore, these fine synchrony events result mostly from transient increases in overall neuronal network spiking rates, rather than changes in precise spiking correlations between specific pairs of neurons.

Original languageEnglish (US)
Pages (from-to)9927-9944
Number of pages18
JournalJournal of Neuroscience
Volume34
Issue number30
DOIs
StatePublished - Jan 1 2014
Externally publishedYes

Keywords

  • Collective dynamics
  • Conditional inference
  • Epilepsy
  • Maximum entropy

ASJC Scopus subject areas

  • Neuroscience(all)

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  • Cite this

    Truccolo, W., Ahmed, O. J., Harrison, M. T., Eskandar, E. N., Rees Cosgrove, G., Madsen, J. R., Blum, A. S., Stevenson Potter, N., Hochberg, L. R., & Cash, S. S. (2014). Neuronal ensemble synchrony during human focal seizures. Journal of Neuroscience, 34(30), 9927-9944. https://doi.org/10.1523/JNEUROSCI.4567-13.2014