Non-REM and REM/paradoxical sleep dynamics across phylogeny

Abstract

All animals carefully studied sleep, suggesting that sleep as a behavioral state exists in all animal life. Such evolutionary maintenance of an otherwise vulnerable period of environmental detachment suggests that sleep must be integral in fundamental biological needs. Despite over a century of research, the knowledge of what sleep does at the tissue, cellular or molecular levels remain cursory. Currently, sleep is defined based on behavioral criteria and physiological measures rather than at the cellular or molecular level. Physiologically, sleep has been described as two main states, non-rapid eye moment (NREM) and REM/paradoxical sleep (PS), which are defined in the neocortex by synchronous oscillations and paradoxical wake-like activity, respectively. For decades, these two sleep states were believed to be defining characteristics of only mammalian and avian sleep. Recent work has revealed slow oscillation, silencing, and paradoxical/REM-like activities in reptiles, fish, flies, worms, and cephalopods suggesting that these sleep dynamics and associated physiological states may have emerged early in animal evolution. Here, we discuss these recent developments supporting the conservation of neural dynamics (silencing, oscillation, paradoxical activity) of sleep states across phylogeny.

Figure 1.

What is sleep? A. Sleep is found in all animals carefully studied so far and shares common traits of quiescence, sensory detachment, metabolic reduction, and homeostasis/circadian regulation. B. Neural signatures of sleep have been found in animals ranging from c. elegans to humans. Three different sleep signatures are known: REM/PS is a state of sleep characterized by wake-like activity in the forebrain, accompanied by muscle twitches, eye movements, and cardiorespiratory fluctuations. Non-REM/SWS is defined by slow, high amplitude bursts in the forebrain, with muscle atonia, and reduced cardio-respiratory rate. Silencing is perhaps the core signature of neural sleep physiology, as it accompanies both REM/PS and Non-REM/SWS in large areas of the brain outside the cortex. C. Sleep physiology in tissues across the body. Sleep can be broken down into tissue/cellular signatures that associate with sleep, which have been found from neurons to muscle. Additionally, sleep can be considered for the genetic regulation that occurs in many tissue types across the body. Lastly, sleep can be examined by the tissue, cellular, and molecular processes that are dependent on proper sleep regulation, which have been found in all major tissue types. See for review of sleep genetics.