Aspects of tree shrew consolidated sleep structure resemble human sleep

Marta M Dimanico,Michael Harvey,Jing Wang,Gregor Rainer,Melanie Kaeser,Björn Rasch,Arndt-Lukas Klaassen

doi:10.1038/s42003-021-02234-7

Marta M Dimanico, Michael Harvey + Show 5 more

Open Access

https://doi.org/10.1038/s42003-021-02234-7

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Abstract

Understanding human sleep requires appropriate animal models. Sleep has been extensively studied in rodents, although rodent sleep differs substantially from human sleep. Here we investigate sleep in tree shrews, small diurnal mammals phylogenetically close to primates, and compare it to sleep in rats and humans using electrophysiological recordings from frontal cortex of each species. Tree shrews exhibited consolidated sleep, with a sleep bout duration parameter, τ, uncharacteristically high for a small mammal, and differing substantially from the sleep of rodents that is often punctuated by wakefulness. Two NREM sleep stages were observed in tree shrews: NREM, characterized by high delta waves and spindles, and an intermediate stage (IS-NREM) occurring on NREM to REM transitions and consisting of intermediate delta waves with concomitant theta-alpha activity. While IS-NREM activity was reliable in tree shrews, we could also detect it in human EEG data, on a subset of transitions. Finally, coupling events between sleep spindles and slow waves clustered near the beginning of the sleep period in tree shrews, paralleling humans, whereas they were more evenly distributed in rats. Our results suggest considerable homology of sleep structure between humans and tree shrews despite the large difference in body mass between these species.

Highlights

Understanding human sleep requires appropriate animal models
We noticed that anterior cingulate cortex (ACC) local field potentials (LFPs) power in the theta-alpha range (4–12 Hz) reliably exhibited notable peaks during the NREM to rapid eye movement (REM) transitions, i.e., during the downward slope of delta power
We present evidence for an intermediate sleep stage that prominently occurs in the tree shrew at transitions between NREM and REM sleep

Summary

Introduction

Understanding human sleep requires appropriate animal models. Sleep has been extensively studied in rodents, rodent sleep differs substantially from human sleep. The discrepancy regarding the main sleep period between humans and laboratory rodents has led researchers to study several mammalian species, whose sleep patterns more closely approximate those of humans One of these diurnal species is the Sudanian grass rat (Arvicanthis ansorgei), a rodent species that spends on average about 50% of the day in the awake state compared to 30% awake time during the night[11]. Rhabdomys appear to be highly sensitive to the rate of luminance change around day/night transitions, such that a gradual illumination change over a 6 h transition period tends to further enhance diurnal locomotor activity patterns These two diurnal rodent species are examples of less frequently used animal models, which provide important comparative perspectives on mammalian sleep

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