Team Memory, Oscillations and Brain States (MOBs), Plasticité du cerveau, ESPCI Paris, CNRS, PSL University, 75005 Paris, France.
PLoS Biol. 2018 Nov 8;16(11):e2005458. doi: 10.1371/journal.pbio.2005458. eCollection 2018 Nov.
Real-time tracking of vigilance states related to both sleep or anaesthesia has been a goal for over a century. However, sleep scoring cannot currently be performed with brain signals alone, despite the deep neuromodulatory transformations that accompany sleep state changes. Therefore, at heart, the operational distinction between sleep and wake is that of immobility and movement, despite numerous situations in which this one-to-one mapping fails. Here we demonstrate, using local field potential (LFP) recordings in freely moving mice, that gamma (50-70 Hz) power in the olfactory bulb (OB) allows for clear classification of sleep and wake, thus providing a brain-based criterion to distinguish these two vigilance states without relying on motor activity. Coupled with hippocampal theta activity, it allows the elaboration of a sleep scoring algorithm that relies on brain activity alone. This method reaches over 90% homology with classical methods based on muscular activity (electromyography [EMG]) and video tracking. Moreover, contrary to EMG, OB gamma power allows correct discrimination between sleep and immobility in ambiguous situations such as fear-related freezing. We use the instantaneous power of hippocampal theta oscillation and OB gamma oscillation to construct a 2D phase space that is highly robust throughout time, across individual mice and mouse strains, and under classical drug treatment. Dynamic analysis of trajectories within this space yields a novel characterisation of sleep/wake transitions: whereas waking up is a fast and direct transition that can be modelled by a ballistic trajectory, falling asleep is best described as a stochastic and gradual state change. Finally, we demonstrate that OB oscillations also allow us to track other vigilance states. Non-REM (NREM) and rapid eye movement (REM) sleep can be distinguished with high accuracy based on beta (10-15 Hz) power. More importantly, we show that depth of anaesthesia can be tracked in real time using OB gamma power. Indeed, the gamma power predicts and anticipates the motor response to stimulation both in the steady state under constant anaesthetic and dynamically during the recovery period. Altogether, this methodology opens the avenue for multi-timescale characterisation of brain states and provides an unprecedented window onto levels of vigilance.
一个多世纪以来,实时跟踪与睡眠或麻醉相关的警觉状态一直是一个目标。然而,尽管睡眠状态变化伴随着深度的神经调制转换,但目前仅凭大脑信号还无法进行睡眠评分。因此,从本质上讲,睡眠和清醒的操作区别在于不动和运动,尽管在许多情况下,这种一一映射并不成立。在这里,我们使用自由活动的小鼠的局部场电位 (LFP) 记录证明,嗅球 (OB) 中的伽马 (50-70 Hz) 功率可以清楚地区分睡眠和清醒,从而提供了一种基于大脑的标准,无需依赖运动活动即可区分这两种警觉状态。与海马 theta 活动相结合,它可以为仅依赖大脑活动的睡眠评分算法的制定提供帮助。这种方法与基于肌肉活动 (肌电图 [EMG]) 和视频跟踪的经典方法的相似度超过 90%。此外,与 EMG 相反,OB 伽马功率允许在类似恐惧相关冻结的模糊情况下正确区分睡眠和不动。我们使用海马 theta 振荡和 OB 伽马振荡的瞬时功率来构建一个 2D 相空间,该相空间在整个时间、个体小鼠和小鼠品系中以及在经典药物治疗下都具有高度的稳健性。在该空间内的轨迹的动态分析产生了睡眠/唤醒转换的新特征:清醒是一个快速而直接的转变,可以通过弹道轨迹来建模,而入睡最好描述为随机和逐渐的状态变化。最后,我们证明 OB 振荡也允许我们跟踪其他警觉状态。非快速眼动 (NREM) 和快速眼动 (REM) 睡眠可以基于 beta (10-15 Hz) 功率进行高精度区分。更重要的是,我们表明可以使用 OB 伽马功率实时跟踪麻醉深度。事实上,在稳定状态下的恒定麻醉和动态恢复期间,伽马功率可以预测和预期对刺激的运动反应。总的来说,这种方法为大脑状态的多时间尺度特征描述开辟了道路,并提供了一个前所未有的警觉水平窗口。
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