Mammalian Sleep Dynamics: How Diverse Features Arise from a Common Physiological Framework

Abstract

Mammalian sleep varies widely, ranging from frequent napping in rodents to consolidated blocks in primates and unihemispheric sleep in cetaceans. In humans, rats, mice and cats, sleep patterns are orchestrated by homeostatic and circadian drives to the sleep–wake switch, but it is not known whether this system is ubiquitous among mammals. Here, changes of just two parameters in a recent quantitative model of this switch are shown to reproduce typical sleep patterns for 17 species across 7 orders. Furthermore, the parameter variations are found to be consistent with the assumptions that homeostatic production and clearance scale as brain volume and surface area, respectively. Modeling an additional inhibitory connection between sleep-active neuronal populations on opposite sides of the brain generates unihemispheric sleep, providing a testable hypothetical mechanism for this poorly understood phenomenon. Neuromodulation of this connection alone is shown to account for the ability of fur seals to transition between bihemispheric sleep on land and unihemispheric sleep in water. Determining what aspects of mammalian sleep patterns can be explained within a single framework, and are thus universal, is essential to understanding the evolution and function of mammalian sleep. This is the first demonstration of a single model reproducing sleep patterns for multiple different species. These wide-ranging findings suggest that the core physiological mechanisms controlling sleep are common to many mammalian orders, with slight evolutionary modifications accounting for interspecies differences.

Quantitative modelling of sleep dynamics

“…Neural mass and neural field models are well suited to exploring the mechanisms that control arousal and related EEG phenomena. The models reviewed here provide a framework for additional applications to phenomena, such as chronic sleep deprivation, and sleep in other species [56]. They also lay the foundation for further generalization and integration of additional physiology, in particular, inclusion and calibration of more realistic circadian inputs via the SCN to treat shiftwork, jetlag and chronotypes, and inclusion of Orx nuclei.…”

Adolescent sleep patterns in humans and laboratory animals

“…The sleep cycles in laboratory rodents are much shorter and take place on the order of minutes. In most species, sleep still predominantly occurs at a particular time of day (day for nocturnal species, night for diurnal species) but it does so stochastically, punctuated by episodes of wake (Kas and Edgar, 1999; Mistlberger, 2005; Phillips et al, 2010; Tobler and Borbeley, 1986). Despite this “polyphasic” pattern of sleeping, SWA still decreases during relatively consolidated periods of sleep, and builds up at times of day characterized by high amounts of waking activity, reflecting sleep pressure (Franken et al, 1991; Tobler and Borbeley, 1986; Tobler et al, 1992).…”

“…This staggered phase relationship produces a consolidated sleep episode (Dijk and Czeisler, 1994). In contrast, in rodents, it is theorized that either a reduced threshold for sleep onset (U), or accelerated time constant for homeostatic build up and dissipation (τi and τd) produces a polyphasic sleep pattern, with a higher density of sleep happening during the peak circadian drive for sleep (Daan et al, 1984; Phillips et al, 2010; Tobler et al, 1992). …”

“…A) To model adolescent changes in the sleep patterns of polyphasic species, such as laboratory rodents, we increased the speed of homeostatic sleep pressure build up and dissipation (Phillips et al, 2010), and then ran a similar set of simulations as humans, but varying the time constants between 50% and 400% of τi = 0.215 h (an instantaneous build up rate of 1.65/h) and τd = 0.606 h (an instantaneous break down rate of 4.65/h). It should be noted that although the time constants for sleep pressure build up and dissipation have not been well-studied in developing rodents, models predict that a 160–200% increase in τ might occur in these small, fast-developing species simply due to brain growth (Phillips et al, 2010) and observations of behavioral and SWA suggest that the ability to tolerate sleep deprivation may increase by 3 to 12-fold (!) in rats between weaning and adulthood (Alfoldi et al, 1990).…”

Predation and the phasing of sleep: an evolutionary individual-based model

“…Sleep also can be investigated using modelling approaches (Mirolli & Parisi 2003;Beckman et al 2007;Lima & Rattenborg 2007;Acerbi et al 2008, Phillips et al 2010. In this paper we describe a simulation model that builds on our previous study of ecological constraints and sleep by including predation risk (Acerbi et al 2008).…”