Patel Mainak, Joshi Badal
Department of Mathematics, William & Mary, Williamsburg, VA, United States.
Department of Mathematics, California State University San Marcos, San Marcos, CA, United States.
Front Netw Physiol. 2024 Jan 4;3:1340722. doi: 10.3389/fnetp.2023.1340722. eCollection 2023.
In early infancy, rats randomly alternate between the sleeping and waking states-from postnatal day 2-10 (P2-P10), sleep and wake bouts are both exponentially distributed with increasing means, while from P10-P21 sleep and wake bout means continue to increase, though there is a striking qualitative shift in the distribution of wake bouts from exponential to power law. The behavioral states of sleep and wakefulness correspond to the activity of sleep-active and wake-active neuronal brainstem populations, with reciprocal inhibition between the two ensuring that only one population is active at a time. The locus coeruleus (LC) forms a third component of this circuit that rises in prominence during the P10-P21 period, as experimental evidence shows that an as-of-yet undeciphered interaction of the LC with sleep-active and wake-active populations is responsible for the transformation of the wake bout distribution from exponential to power law. Interestingly, the LC undergoes remarkable physiological changes during the P10-P21 period-gap junctions within the LC are pruned and network-wide oscillatory synchrony declines and vanishes. In this work, we discuss a series of models of sleep-active, wake-active, and the LC populations, and we use these models to postulate the nature of the interaction between these three populations and how these interactions explain empirical observations of sleep and wake bout dynamics. We hypothesize a circuit in which there is reciprocal excitation between the LC and wake-active population with inhibition from the sleep-active population to the LC that suppresses the LC during sleep bouts. During the P2-P10 period, we argue that a noise-based switching mechanism between the sleep-active and wake-active populations provides a simple and natural way to account for exponential bout distributions, and that the locked oscillatory state of the LC prevents it from impacting bout distributions. From P10-P21, we use our models to postulate that, as the LC gradually shifts from a state of synchronized oscillations to a state of continuous firing, reciprocal excitation between the LC and the wake-active population is able to gradually transform the wake bout distribution from exponential to power law.
在婴儿早期,大鼠在睡眠和清醒状态之间随机交替——从出生后第2天到第10天(P2 - P10),睡眠和清醒时段均呈指数分布,且均值不断增加,而从P10到P21,睡眠和清醒时段的均值继续增加,不过清醒时段的分布从指数分布到幂律分布发生了显著的质的转变。睡眠和清醒的行为状态对应于睡眠活跃和清醒活跃的脑干神经元群体的活动,两者之间的相互抑制确保了每次只有一个群体处于活跃状态。蓝斑(LC)构成了该回路的第三个组成部分,在P10 - P21期间变得突出,因为实验证据表明,LC与睡眠活跃和清醒活跃群体之间尚未破译的相互作用导致了清醒时段分布从指数分布转变为幂律分布。有趣的是,LC在P10 - P21期间经历了显著的生理变化——LC内的缝隙连接被修剪,全网络的振荡同步性下降并消失。在这项工作中,我们讨论了一系列关于睡眠活跃、清醒活跃和LC群体的模型,并使用这些模型推测这三个群体之间相互作用的性质,以及这些相互作用如何解释睡眠和清醒时段动态的实证观察结果。我们假设了一个回路,其中LC和清醒活跃群体之间存在相互兴奋,而睡眠活跃群体对LC有抑制作用,在睡眠时段抑制LC。在P2 - P10期间,我们认为睡眠活跃和清醒活跃群体之间基于噪声的切换机制为指数时段分布提供了一种简单而自然的解释方式,并且LC的锁定振荡状态使其无法影响时段分布。从P10到P21,我们使用模型推测,随着LC逐渐从同步振荡状态转变为持续放电状态,LC与清醒活跃群体之间的相互兴奋能够逐渐将清醒时段分布从指数分布转变为幂律分布。