Roles for Sleep in Neural and Behavioral Plasticity: Reviewing Variation in the Consequences of Sleep Loss

Abstract

Sleep is a vital physiological state that has been broadly conserved across the evolution of animal species. While the precise functions of sleep remain poorly understood, a large body of research has examined the negative consequences of sleep loss on neural and behavioral plasticity. While sleep disruption generally results in degraded neural plasticity and cognitive function, the impact of sleep loss can vary widely with age, between individuals, and across physiological contexts. Additionally, several recent studies indicate that sleep loss differentially impacts distinct neuronal populations within memory-encoding circuitry. These findings indicate that the negative consequences of sleep loss are not universally shared, and that identifying conditions that influence the resilience of an organism (or neuron type) to sleep loss might open future opportunities to examine sleep's core functions in the brain. Here, we discuss the functional roles for sleep in adaptive plasticity and review factors that can contribute to individual variations in sleep behavior and responses to sleep loss.

Human REM sleep controls neural excitability in support of memory formation

“…During wakefulness and learning, new synapses are formed, existing connections are strengthened and overall neural firing increases, thus, resulting in an accumulation of excitation with time spent awake (Maret et al, 2011; Vyazovskiy et al, 2008, 2009). Sleep has been proposed to counteract this progressive build-up of excitation to maintain healthy neural functioning, with sleep deprivation attenuating such homeostatic regulation and impairing cognitive processes and memory formation (Huber et al, 2013; Vyazovskiy et al, 2009; Weiss and Donlea, 2022).…”

“…Sleep has been proposed to counteract this progressive build-up of excitation to maintain healthy neural functioning, with sleep deprivation attenuating such homeostatic regulation and impairing cognitive processes and memory formation (Huber et al, 2013;Vyazovskiy et al, 2009;Weiss and Donlea, 2022).…”

“…Related, in vivo animals studies have revealed that wakefulness and learning lead to a progressive build-up of cellular synaptic potentiation and a net increase of excitability (Tononi and Cirelli, 2014; Vyazovskiy et al, 2008, 2009). In extreme, prolonged wakefulness using sleep deprivation in animal models impairs memory performance due to synaptic saturation (Huber et al, 2013; Weiss and Donlea, 2022). It has been proposed that, during sleep, a neural homeostatic process restores the optimal neural milieu for learning (Timofeev et al, 2001; Tononi and Cirelli, 2006, 2014).…”

Dynamics of sleep, feeding, and metabolic homeostasis inDrosophilaensheathing glia, astrocytes, and neurons

“…Sleep is important for a number of processes in the brain, many of which are related to plastic changes, such as learning and memory or clearing of waste products 4, 14, 15 . Vice versa , the experience during wakefulness, in particular the duration of time spent awake, but also for example learning or injury, impact subsequent sleep across species 4, 15 . However, how neural circuits in the brain integrate the time spent awake as well as specific behaviors for homeostatic sleep regulation, is little understood 3–6 .…”

“…Ensheathing glia therefore act as a system for sleep control distributed across brain areas. The structural arrangement of these glia suggests that sleep homeostasis differentially impacts large ensembles of cells at the same time.Sleep is important for a number of processes in the brain, many of which are related to plastic changes, such as learning and memory or clearing of waste products 4,14,15 . Vice versa, the experience during wakefulness, in particular the duration of time spent awake, but also for example learning or injury, impact subsequent sleep across species 4, 15 .…”