RT Journal Article
SR Electronic
T1 REM sleep sawtooth waves are associated with widespread cortical activations
JF The Journal of Neuroscience
JO J. Neurosci.
FD Society for Neuroscience
SP JN-RM-1586-20
DO 10.1523/JNEUROSCI.1586-20.2020
A1 Birgit Frauscher
A1 Nicolás von Ellenrieder
A1 Irena Dolezalova
A1 Sarah Bouhadoun
A1 Jean Gotman
A1 Laure Peter-Derex
YR 2020
UL http://www.jneurosci.org/content/early/2020/10/13/JNEUROSCI.1586-20.2020.abstract
AB Sawtooth waves (STW) are bursts of frontocentral slow oscillations recorded in the scalp EEG during rapid-eye-movement (REM) sleep. Little is known about their cortical generators and functional significance. Stereo-electroencephalography performed for presurgical epilepsy evaluation offers the unique possibility to study neurophysiology in-situ in the human brain. We investigated intracranial correlates of scalp-detected STW in 26 patients (14 women) undergoing combined stereo-electroencephalography/polysomnography. We visually marked STW segments in scalp EEG and selected stereo-electroencephalography channels exhibiting normal activity for intracranial analyses. Channels were grouped in 30 brain regions. The spectral power in each channel and frequency band was computed during STW and non-STW control segments. Ripples (80-250 Hz) were automatically detected during STW and control segments. The spectral power in the different frequency bands and the ripple rates were then compared between STW and control segments in each brain region. An increase in 2-4 Hz power during STW segments was found in all brain regions except the occipital lobe, with large effect sizes in the parieto-temporal junction, the lateral and orbital frontal cortex, the anterior insula and mesiotemporal structures. A widespread increase in high frequency activity including ripples was observed concomitantly, involving the sensorimotor cortex, associative areas and limbic structures. This distribution showed a high spatiotemporal heterogeneity. Our results suggest that STW are associated with widely distributed but locally regulated REM sleep slow oscillations. By driving fast activities, STW may orchestrate synchronized reactivations of multifocal activities, allowing tagging of complex representations necessary for REM sleep-dependent memory consolidation.SIGNIFICANCE STATEMENTSawtooth waves (STW) present as scalp EEG bursts of slow waves contrasting with the low-voltage fast desynchronized activity of rapid eye movement (REM) sleep. Little is known about their cortical origin and function. Using combined stereo-electroencephalography/polysomnography possible only in the human brain during presurgical epilepsy evaluation, we explored the intracranial correlates of STW. We found that a large set of regions in the parietal, frontal and insular cortices shows increases in 2-4 Hz power during scalp EEG STW, that STW are associated with a strong and widespread increase in high-frequencies and that these slow and fast activities exhibit a high spatiotemporal heterogeneity. These electrophysiological properties suggest that STW may be involved in cognitive processes during REM sleep.