Evidence for consolidation of neuronal assemblies after seizures in humans

Mark R. Bower, Squire Matthew Stead, Regina S. Bower, Michal T. Kucewicz, Vlastimil Sulc, Jan Cimbalnik, Benjamin Brinkmann, Vincent M. Vasoli, Erik K St Louis, Fredric B. Meyer, W. Richard Marsh, Gregory Alan Worrell

Research output: Contribution to journalArticle

24 Citations (Scopus)

Abstract

The establishment of memories involves reactivation of waking neuronal activity patterns and strengthening of associated neural circuits during slow-wave sleep (SWS), a process known as “cellular consolidation” (Dudai and Morris, 2013). Reactivation of neural activity patterns during waking behaviors that occurs on a timescale of seconds to minutes is thought to constitute memory recall (O’Keefe and Nadel, 1978), whereas consolidation of memory traces may be revealed and served by correlated firing (reactivation) that appears during sleep under conditions suitable for synaptic modification (Buhry et al., 2011). Although reactivation has been observed in human neuronal recordings (Gelbard-Sagiv et al., 2008; Miller et al., 2013), reactivation during sleep has not, likely because data are difficult to obtain and the effect is subtle. Seizures, however, provide intense and synchronous, yet sparse activation (Bower et al., 2012) that could produce a stronger consolidation effect if seizures activate learning-related mechanisms similar to those activated by learned tasks. Continuous wide-bandwidth recordings from patients undergoing intracranial monitoring for drug-resistant epilepsy revealed reactivation of seizure-related neuronal activity during subsequent SWS, but not wakefulness. Those neuronal assemblies that were most strongly activated during seizures showed the largest correlation changes, suggesting that consolidation selectively strengthened neuronal circuits activated by seizures. These results suggest that seizures “hijack” physiological learning mechanisms and also suggest a novel epilepsy therapy targeting neuronal dynamics during post-seizure sleep.

Original languageEnglish (US)
Pages (from-to)999-1010
Number of pages12
JournalJournal of Neuroscience
Volume35
Issue number3
DOIs
StatePublished - Jan 21 2015

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Seizures
Sleep
Learning
Wakefulness
Epilepsy

Keywords

  • Consolidation
  • Epilepsy
  • Learning
  • Memory
  • Neural assemblies
  • Seizures

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Evidence for consolidation of neuronal assemblies after seizures in humans. / Bower, Mark R.; Stead, Squire Matthew; Bower, Regina S.; Kucewicz, Michal T.; Sulc, Vlastimil; Cimbalnik, Jan; Brinkmann, Benjamin; Vasoli, Vincent M.; St Louis, Erik K; Meyer, Fredric B.; Marsh, W. Richard; Worrell, Gregory Alan.

In: Journal of Neuroscience, Vol. 35, No. 3, 21.01.2015, p. 999-1010.

Research output: Contribution to journalArticle

Bower, MR, Stead, SM, Bower, RS, Kucewicz, MT, Sulc, V, Cimbalnik, J, Brinkmann, B, Vasoli, VM, St Louis, EK, Meyer, FB, Marsh, WR & Worrell, GA 2015, 'Evidence for consolidation of neuronal assemblies after seizures in humans', Journal of Neuroscience, vol. 35, no. 3, pp. 999-1010. https://doi.org/10.1523/JNEUROSCI.3019-14.2015
Bower, Mark R. ; Stead, Squire Matthew ; Bower, Regina S. ; Kucewicz, Michal T. ; Sulc, Vlastimil ; Cimbalnik, Jan ; Brinkmann, Benjamin ; Vasoli, Vincent M. ; St Louis, Erik K ; Meyer, Fredric B. ; Marsh, W. Richard ; Worrell, Gregory Alan. / Evidence for consolidation of neuronal assemblies after seizures in humans. In: Journal of Neuroscience. 2015 ; Vol. 35, No. 3. pp. 999-1010.
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