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Rapid Eye Movement Sleep Sawtooth Waves Are Associated with Widespread Cortical Activations
Journal of Neuroscience ( IF 5.3 ) Pub Date : 2020-11-11 , DOI: 10.1523/jneurosci.1586-20.2020
Birgit Frauscher , Nicolás von Ellenrieder , Irena Dolezalova , Sarah Bouhadoun , Jean Gotman , Laure Peter-Derex

Sawtooth waves (STW) are bursts of frontocentral slow oscillations recorded in the scalp electroencephalogram (EEG) during rapid eye movement (REM) sleep. Little is known about their cortical generators and functional significance. Stereo-EEG 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-EEG/polysomnography. We visually marked STW segments in scalp EEG and selected stereo-EEG 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 parietotemporal 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 STATEMENT Sawtooth waves (STW) present as scalp electroencephalographic (EEG) bursts of slow waves contrasting with the low-voltage fast desynchronized activity of REM sleep. Little is known about their cortical origin and function. Using combined stereo-EEG/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.



中文翻译:

快速眼动睡眠锯齿波与广泛的皮层激活有关。

锯齿波(STW)是快速眼动(REM)睡眠期间记录在头皮脑电图(EEG)中的额中央慢振动的爆发。关于它们的皮层生成器及其功能意义知之甚少。用于手术前癫痫评估的立体脑电图为原位研究神经生理学提供了独特的可能性在人脑中。我们调查了26例接受立体脑电图/多导睡眠图检查的患者(14名妇女)的头皮检测到的STW的颅内相关性。我们在头皮脑电图和选定的立体脑电图通道中显示出正常的颅内分析活动,在视觉上标记STW段。通道分为30个大脑区域。在STW和非STW控制段期间计算每个通道和频带中的频谱功率。在STW和控制段期间会自动检测到波纹(80-250 Hz)。然后在每个脑区域的STW和控制段之间比较不同频带中的频谱功率和脉动速率。在STW段期间,除了枕叶外,在所有大脑区域都发现2-4 Hz功率增加,在顶颞交界处有较大的影响,外侧和眶额叶皮层,前岛和中颞结构。同时观察到高频活动的广泛增加,包括波纹,涉及感觉运动皮层,缔合区和边缘结构。这种分布显示出很高的时空异质性。我们的结果表明,STW与广泛分布但局部调节的REM睡眠缓慢振荡有关。通过推动快速活动,STW可以协调多焦点活动的同步重新激活,从而允许对依赖REM睡眠的记忆整合进行必要的复杂表示进行标记。关联区域和边缘结构。这种分布显示出很高的时空异质性。我们的结果表明,STW与广泛分布但局部调节的REM睡眠缓慢振荡有关。通过推动快速活动,STW可以协调多焦点活动的同步重新激活,从而允许对依赖REM睡眠的记忆整合进行必要的复杂表示进行标记。关联区域和边缘结构。这种分布显示出很高的时空异质性。我们的结果表明,STW与广泛分布但局部调节的REM睡眠缓慢振荡有关。通过推动快速活动,STW可以协调多焦点活动的同步重新激活,从而允许对依赖REM睡眠的记忆整合进行必要的复杂表示进行标记。

意义声明锯齿波(STW)以慢波的头皮脑电图(EEG)爆发形式出现,与REM睡眠的低压快速失步活动形成鲜明对比。关于它们的皮质起源和功能知之甚少。使用联合立体脑电图/多导睡眠图可能仅在术前癫痫评估期间在人脑中,我们探讨了STW的颅内相关性。我们发现,在头皮脑电图STW期间,顶叶,额叶和岛状皮质的大量区域显示2-4 Hz功率增加,STW与高频的强烈而普遍的增加相关,并且这些速度缓慢而快速活动表现出很高的时空异质性。这些电生理特性表明,STW可能参与了REM睡眠期间的认知过程。

更新日期:2020-11-12
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