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Role of the Locus Coeruleus Arousal Promoting Neurons in Maintaining Brain Criticality across the Sleep-Wake Cycle
Journal of Neuroscience ( IF 4.4 ) Pub Date : 2024-08-28 , DOI: 10.1523/jneurosci.1939-23.2024
Chengyu Huo 1, 2 , Fabrizio Lombardi 3, 4 , Carlos Blanco-Centurion 5 , Priyattam J Shiromani 5, 6 , Plamen Ch Ivanov 3, 7, 8
Affiliation  

Sleep control depends on a delicate interplay among brain regions. This generates a complex temporal architecture with numerous sleep-stage transitions and intermittent fluctuations to micro-states and brief arousals. These temporal dynamics exhibit hallmarks of criticality, suggesting that tuning to criticality is essential for spontaneous sleep-stage and arousal transitions. However, how the brain maintains criticality remains not understood. Here, we investigate - and -burst dynamics during the sleep–wake cycle of rats (Sprague–Dawley, adult male) with lesion in the wake-promoting locus coeruleus (LC). We show that, in control rats, - and -bursts exhibit power-law (-bursts, active phase) and exponential-like (-bursts, quiescent phase) duration distributions, as well as power-law long-range temporal correlations (LRTCs)—typical of non-equilibrium systems self-organizing at criticality. Furthermore, consecutive - and -bursts durations are characterized by anti-correlated coupling, indicating a new class of self-organized criticality that emerges from underlying feedback between neuronal populations and brain areas involved in generating arousals and sleep states. In contrast, we uncover that LC lesion leads to alteration of - and -burst critical features, with change in duration distributions and correlation properties, and increase in coupling. Notably, these LC-lesion effects are opposite to those observed for lesions in the sleep-promoting ventrolateral preoptic (VLPO) nucleus. Our findings indicate that critical dynamics of - and -bursts arise from a balanced interplay of LC and VLPO, which maintains brain tuning to criticality across the sleep–wake cycle—a non-equilibrium behavior in sleep micro-architecture at short timescales that coexists with large-scale sleep–wake homeostasis.



中文翻译:


蓝斑唤醒促进神经元在整个睡眠-觉醒周期中维持大脑临界性中的作用



睡眠控制取决于大脑区域之间微妙的相互作用。这产生了一个复杂的时间结构,具有大量的睡眠阶段转换和微状态的间歇性波动和短暂的唤醒。这些时间动态表现出关键性的特征,表明调整到关键性对于自发的睡眠阶段和觉醒过渡至关重要。然而,大脑如何保持临界状态仍不清楚。在这里,我们研究了促醒蓝斑(LC)损伤的大鼠(Sprague-Dawley,成年雄性)在睡眠-觉醒周期中的-和-爆发动态。我们发现,在对照大鼠中,-和-爆发表现出幂律(-爆发,活跃期)和指数状(-爆发,静止期)持续时间分布,以及幂律长程时间相关性(LRTC) )——典型的非平衡系统在临界点自组织。此外,连续的 - 和 - 突发持续时间的特征是反相关耦合,表明一种新的自组织临界性,是由神经元群体和参与产生唤醒和睡眠状态的大脑区域之间的潜在反馈产生的。相比之下,我们发现 LC 损伤会导致 - 和 - 突发关键特征的改变,随着持续时间分布和相关属性的变化,以及 - 耦合的增加。值得注意的是,这些 LC 损伤效应与促睡眠腹外侧视前核 (VLPO) 损伤中观察到的效应相反。 我们的研究结果表明,-和-突发的关键动态源于 LC 和 VLPO 的平衡相互作用,这使大脑在整个睡眠-觉醒周期中保持临界状态——睡眠微架构中短时间尺度上的一种非平衡行为,与大规模的睡眠-觉醒稳态。

更新日期:2024-08-29
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