The sleep–wake cycle in adult rats following pilocarpine-induced temporal lobe epilepsy

Matos, Gabriela; Tsai, Rodrigo; Baldo, Marcus Vinícius C.; Castro, Isac de; Sameshima, Koichi; Valle, Angela C.

doi:10.1016/j.yebeh.2009.11.015

Cited by 28 publications

(36 citation statements)

References 41 publications

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“…Our findings are in contrast to the growing consensus (Malow, 2007;Kothare and Zarowki, 2011;Derry and Duncan, 2013;Dewolfe et al, 2013, Ng andPavlova, 2013) that NREM and relaxed wake states permit and REM and active wake states prevent epileptic seizures. These notions emerge, in part, from seminal studies in the cat penicillin and amygdala kindling models of epilepsy by Shouse (1987) and Shouse et al (1989Shouse et al ( , 1990Shouse et al ( , 2000 in which a majority of seizures emerged from NREM and few seizures emerged from REM, attributed to differences in cortical synchrony between these states (Shouse et al, 1989(Shouse et al, , 2000but see Sinha, 2011).…”

Section: Discussioncontrasting

confidence: 99%

“…There is an acknowledged relationship between state of vigilance (SOV), also known as sleep-wake state, and seizure onset in various human (Bazil and Walczak, 1997;Crespel et al, 2000;for review, see Dinner, 2002;Minecan et al, 2002;Malow, 2007;Kothare and Zarowki, 2011;Sinha, 2011) and experimental (Quigg et al, 2000;Shouse et al, 2000;Colom et al, 2006; for review, see Matos et al, 2011;Sinha, 2011) epilepsies. Additionally, epilepsy, in turn, alters sleep patterns (Cepeda et al, 1982;Ayala-Guerro et al, 2002;Matos et al, 2010; for review, see Matos et al, 2011).…”

Section: Introductionmentioning

confidence: 99%

“…Additionally, epilepsy, in turn, alters sleep patterns (Cepeda et al, 1982;Ayala-Guerro et al, 2002;Matos et al, 2010; for review, see Matos et al, 2011). Different SOVs are accompanied by changes in synaptic transmission and patterns of network activity in the brain (Loddenkemper et al, 2011;Sinha, 2011).…”

Section: Introductionmentioning

confidence: 99%

“…Thus, although we do not yet understand the mechanisms of this interaction, the observed effect of SOV on seizure onset is not surprising given our knowledge of sleep-wake networks. Despite the availability of several animal models of epilepsy (Buckmaster, 2004;Soltesz and Staley, 2008), the effect of sleep in epilepsy remains relatively unexplored (Malow, 2007;Matos et al, 2011;Dewolfe et al, 2013).…”

Section: Introductionmentioning

confidence: 99%

“…There is consensus that epileptic seizures often arise from nonrapid eye movement sleep (NREM) and relaxed wake and rarely from rapid eye movement sleep (REM) or active wake states in animals (Miller et al, 1994;Shouse et al, 2000;Colom et al, 2006) and humans (Crespel et al, 2000;Herman et al, 2001;Minecan et al, 2002;Malow 2007;Ng and Pavlova, 2013). However, the relationships between SOV and seizure onset seem to be dependent on the etiology of the epilepsy model or syndrome.…”

Section: Introductionmentioning

confidence: 99%

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

Sedigh-Sarvestani¹,

Thuku²,

Sunderam³

et al. 2014

J. Neurosci.

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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 ϳ90 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.

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Section: Discussioncontrasting

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 3 more Smart Citations

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

Sedigh-Sarvestani¹,

Thuku²,

Sunderam³

et al. 2014

J. Neurosci.

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A companion to the preclinical common data elements and case report forms for rodent EEG studies. A report of the TASK3 EEG Working Group of the ILAE/AES Joint Translational Task Force

et al. 2018

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SummaryElectroencephalography (EEG) is commonly used in epilepsy and neuroscience research to study brain activity. The principles of EEG recording such as signal acquisition, digitization, and conditioning share similarities between animal and clinical EEG systems. In contrast, preclinical EEG studies demonstrate more variability and diversity than clinical studies in the types and locations of EEG electrodes, methods of data analysis, and scoring of EEG patterns and associated behaviors. The TASK3 EEG working group of the International League Against Epilepsy/American Epilepsy Society (ILAE/AES) Joint Translational Task Force has developed a set of preclinical common data elements (CDEs) and case report forms (CRFs) for recording, analysis, and scoring of animal EEG studies. This companion document accompanies the first set of proposed preclinical EEG CRFs and is intended to clarify the CDEs included in these worksheets. We provide 7 CRF and accompanying CDE modules for use by the research community, covering video acquisition, electrode information, experimental scheduling, and scoring of EEG activity. For ease of use, all data elements and input ranges are defined in supporting Excel charts (Appendix S1).

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Cognitive impairment in temporal lobe epilepsy: Role of online and offline processing of single cell information

et al. 2014

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Cognitive impairment is a common comorbidity in temporal lobe epilepsy (TLE) and is often considered more detrimental to quality of life than seizures. While it has been previously shown that the encoding of memory during behavior is impaired in the pilocarpine model of TLE in rats, how this information is consolidated during the subsequent sleep period remains unknown. In this study, we first report marked deficits in spatial memory performance and severe cell loss in the CA1 layer of the hippocampus lower spatial coherence of firing in TLE rats. We then present the first evidence that the reactivation of behavior-driven patterns of activity of CA1 place cells in the hippocampus is intact in TLE rats. Using a template-matching method, we discovered that real-time (3–5 s) reactivation structure was intact in TLE rats. Furthermore, we estimated the entropy rate of short time scale (~250 ms) bursting activity using block entropies and found that significant, extended temporal correlations exist in both TLE and Control rats. Fitting a first order Markov Chain model to these bursting time series, we found that long sequences derived from behavior were significantly enriched in the Markov model over corresponding models fit on randomized data confirming the presence of replay in shorter time scales. We propose that the persistent consolidation of poor spatial information in both real-time and during bursting activity may contribute to memory impairments in TLE rats.

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The sleep–wake cycle in adult rats following pilocarpine-induced temporal lobe epilepsy

Cited by 28 publications

References 41 publications

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

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

A companion to the preclinical common data elements and case report forms for rodent EEG studies. A report of the TASK3 EEG Working Group of the ILAE/AES Joint Translational Task Force

Cognitive impairment in temporal lobe epilepsy: Role of online and offline processing of single cell information

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