Andrillon Thomas, Poulsen Andreas Trier, Hansen Lars Kai, Léger Damien, Kouider Sid
Brain and Consciousness Group, Département d'Études Cognitives, École Normale Supérieure, PSL Research University, 75005 Paris, France, École Doctorale Cerveau Cognition Comportement, Université Pierre et Marie Curie, 75005 Paris, France,
Technical University of Denmark, DTU Compute, 2800 Lyngby, Denmark, and.
J Neurosci. 2016 Jun 15;36(24):6583-96. doi: 10.1523/JNEUROSCI.0902-16.2016.
Sleep is characterized by a loss of behavioral responsiveness. However, recent research has shown that the sleeping brain is not completely disconnected from its environment. How neural activity constrains the ability to process sensory information while asleep is yet unclear. Here, we instructed human volunteers to classify words with lateralized hand responses while falling asleep. Using an electroencephalographic (EEG) marker of motor preparation, we show how responsiveness is modulated across sleep. These modulations are tracked using classic event-related potential analyses complemented by Lempel-Ziv complexity (LZc), a measure shown to track arousal in sleep and anesthesia. Neural activity related to the semantic content of stimuli was conserved in light non-rapid eye movement (NREM) sleep. However, these processes were suppressed in deep NREM sleep and, importantly, also in REM sleep, despite the recovery of wake-like neural activity in the latter. In NREM sleep, sensory activations were counterbalanced by evoked down states, which, when present, blocked further processing of external information. In addition, responsiveness markers correlated positively with baseline complexity, which could be related to modulation in sleep depth. In REM sleep, however, this relationship was reversed. We therefore propose that, in REM sleep, endogenously generated processes compete with the processing of external input. Sleep can thus be seen as a self-regulated process in which external information can be processed in lighter stages but suppressed in deeper stages. Last, our results suggest drastically different gating mechanisms in NREM and REM sleep.
Previous research has tempered the notion that sleepers are isolated from their environment. Here, we pushed this idea forward and examined, across all sleep stages, the brain's ability to flexibly process sensory information, up to the decision level. We extracted an EEG marker of motor preparation to determine the completion of the sensory processing chain and explored how it is constrained by baseline and evoked neural activity. In NREM sleep, slow waves elicited by stimuli appeared to block response preparation. We also used a novel analytic approach (Lempel-Ziv complexity) and showed that the ability to process external information correlates with neural complexity. A reversal of the correlation between complexity and motor indices in REM sleep suggests drastically different gating mechanisms across sleep stages.
睡眠的特征是行为反应性丧失。然而，最近的研究表明，睡眠中的大脑并未完全与外界环境隔绝。目前尚不清楚神经活动如何在睡眠期间限制处理感觉信息的能力。在此，我们指导人类志愿者在入睡过程中用偏向一侧的手部反应对单词进行分类。利用运动准备的脑电图（EEG）标记，我们展示了反应性在睡眠过程中是如何被调节的。这些调节通过经典的事件相关电位分析并辅以莱姆普尔-齐夫复杂度（LZc）来追踪，LZc是一种已被证明可追踪睡眠和麻醉状态下觉醒程度的指标。与刺激语义内容相关的神经活动在浅度非快速眼动（NREM）睡眠中得以保留。然而，这些过程在深度NREM睡眠中受到抑制，重要的是，在快速眼动（REM）睡眠中也受到抑制，尽管后者恢复了类似清醒时的神经活动。在NREM睡眠中，感觉激活被诱发的下行状态所抵消，当下行状态出现时，会阻断对外部信息的进一步处理。此外，反应性标记与基线复杂度呈正相关，这可能与睡眠深度的调节有关。然而，在REM睡眠中，这种关系则相反。因此，我们提出，在REM睡眠中，内源性产生的过程与外部输入的处理相互竞争。因此，睡眠可被视为一个自我调节的过程，在较浅阶段可以处理外部信息，而在较深阶段则受到抑制。最后，我们的结果表明NREM和REM睡眠中的门控机制截然不同。
先前的研究缓和了睡眠者与外界环境隔绝的观念。在此，我们进一步推进这一观点，并在所有睡眠阶段研究大脑灵活处理感觉信息直至决策层面的能力。我们提取了运动准备的EEG标记以确定感觉处理链的完成情况，并探究其如何受到基线和诱发神经活动的限制。在NREM睡眠中，刺激引发的慢波似乎会阻断反应准备。我们还使用了一种新颖的分析方法（莱姆普尔-齐夫复杂度），并表明处理外部信息的能力与神经复杂度相关。REM睡眠中复杂度与运动指标之间相关性的逆转表明不同睡眠阶段的门控机制截然不同。
