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Articles, Neurobiology of Disease

Rapid Eye Movement Sleep and Hippocampal Theta Oscillations Precede Seizure Onset in the Tetanus Toxin Model of Temporal Lobe Epilepsy

Madineh Sedigh-Sarvestani, Godfrey I. Thuku, Sridhar Sunderam, Anjum Parkar, Steven L. Weinstein, Steven J. Schiff and Bruce J. Gluckman
Journal of Neuroscience 22 January 2014, 34 (4) 1105-1114; https://doi.org/10.1523/JNEUROSCI.3103-13.2014
Madineh Sedigh-Sarvestani
1Center for Neural Engineering, Departments of Engineering Science and Mechanics,
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Godfrey I. Thuku
1Center for Neural Engineering, Departments of Engineering Science and Mechanics,
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Sridhar Sunderam
1Center for Neural Engineering, Departments of Engineering Science and Mechanics,
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Anjum Parkar
1Center for Neural Engineering, Departments of Engineering Science and Mechanics,
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Steven L. Weinstein
5Children's National Medical Center, George Washington University, Washington, DC 20010
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Steven J. Schiff
1Center for Neural Engineering, Departments of Engineering Science and Mechanics,
2Neurosurgery,
3Physics, and
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Bruce J. Gluckman
1Center for Neural Engineering, Departments of Engineering Science and Mechanics,
2Neurosurgery,
4Bioengineering, Pennsylvania State University, University Park, Pennsylvania 16802, and
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Abstract

Improved understanding of the interaction between state of vigilance (SOV) and seizure onset has therapeutic potential. Six rats received injections of tetanus toxin (TeTX) in the ventral hippocampus that resulted in chronic spontaneous seizures. The distribution of SOV before 486 seizures was analyzed for a total of 19 d of recording. Rapid eye movement sleep (REM) and exploratory wake, both of which express prominent hippocampal theta rhythm, preceded 47 and 34%, for a total of 81%, of all seizures. Nonrapid eye movement sleep (NREM) and nonexploratory wake, neither of which expresses prominent theta, preceded 6.8 and 13% of seizures. We demonstrate that identification of SOV yields significant differentiation of seizure susceptibilities, with the instantaneous seizure rate during REM nearly 10 times higher than baseline and the rate for NREM less than half of baseline. Survival analysis indicated a shorter duration of preseizure REM bouts, with a maximum transition to seizure at ∼90 s after the onset of REM. This study provides the first analysis of a correlation between SOV and seizure onset in the TeTX model of temporal lobe epilepsy, as well as the first demonstration that hippocampal theta rhythms associated with natural behavioral states can serve a seizure-promoting role. Our findings are in contrast with previous studies suggesting that the correlations between SOV and seizures are primarily governed by circadian oscillations and the notion that hippocampal theta rhythms inhibit seizures. The documentation of significant SOV-dependent seizure susceptibilities indicates the potential utility of SOV and its time course in seizure prediction and control.

  • epilepsy
  • hippocampal theta
  • preseizure state
  • rapid eye movement
  • sleep
  • tetanus toxin
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The Journal of Neuroscience: 34 (4)
Journal of Neuroscience
Vol. 34, Issue 4
22 Jan 2014
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Rapid Eye Movement Sleep and Hippocampal Theta Oscillations Precede Seizure Onset in the Tetanus Toxin Model of Temporal Lobe Epilepsy
Madineh Sedigh-Sarvestani, Godfrey I. Thuku, Sridhar Sunderam, Anjum Parkar, Steven L. Weinstein, Steven J. Schiff, Bruce J. Gluckman
Journal of Neuroscience 22 January 2014, 34 (4) 1105-1114; DOI: 10.1523/JNEUROSCI.3103-13.2014

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Rapid Eye Movement Sleep and Hippocampal Theta Oscillations Precede Seizure Onset in the Tetanus Toxin Model of Temporal Lobe Epilepsy
Madineh Sedigh-Sarvestani, Godfrey I. Thuku, Sridhar Sunderam, Anjum Parkar, Steven L. Weinstein, Steven J. Schiff, Bruce J. Gluckman
Journal of Neuroscience 22 January 2014, 34 (4) 1105-1114; DOI: 10.1523/JNEUROSCI.3103-13.2014
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Keywords

  • epilepsy
  • hippocampal theta
  • preseizure state
  • rapid eye movement
  • sleep
  • tetanus toxin

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