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

Andrew J K Phillips,Romesh G Abeysuriya,David J Kedziora,Peter A Robinson,Karl J Friston

doi:10.1371/journal.pcbi.1000826

Andrew J K Phillips, Romesh G Abeysuriya + Show 3 more

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https://doi.org/10.1371/journal.pcbi.1000826

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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.

Highlights

The diversity of mammalian sleep poses a great challenge to those studying the nature and function of sleep
These parameters were: (i) the homeostatic time constant, determining the rate of somnogen accumulation and clearance, and (ii) the mean drive to the ventrolateral preoptic area of the hypothalamus (VLPO), provided by the suprachiasmatic nucleus (SCN), dorsomedial hypothalamus (DMH) and other neuronal populations
The homeostatic time constant was found previously to be approximately 45 h for humans, based on the rate of recovery from total sleep deprivation [19], but we found here that reducing it below 16 h resulted in polyphasic sleep, as seen in most other mammals

Summary

Introduction

The diversity of mammalian sleep poses a great challenge to those studying the nature and function of sleep. Typical daily sleep durations range from 3 h in horses to 19 h in bats [1,2], which has led to recent speculation that sleep has no universal function beyond timing environmental interactions, with its character defined purely by ecological adaptations on a species-by-species basis [3]. Some aquatic mammals (such as dolphins and seals) engage in unihemispheric sleep, whereby they sleep with only one brain hemisphere at a time [4,5,6]. This behavior appears to serve several functions, including improved environmental surveillance and sensory processing, and respiratory maintenance [7], the physiological mechanism is unknown [8,9]. Mammalian sleep is remarkably diverse in expression, it is very likely universal in origin

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