Dormir ou não dormir, eis a questão...

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

Andrew J. K. Phillips1,2,3*, Peter A. Robinson1,2,4, David J. Kedziora1,2, Romesh G. Abeysuriya1,2

1 School of Physics, University of Sydney, Sydney, Australia, 2Brain Dynamics Center, Westmead Millennium Institute, Sydney Medical School - Western, University of Sydney, Westmead Hospital, Sydney, Australia, 3 Division of Sleep Medicine, Brigham & Women's Hospital, Harvard Medical School, Boston, Massachussetts, United States of America, 4 Center for Integrated Research and Understanding of Sleep, Camperdown, Australia

Abstract Top

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.

Author Summary Top

The field of sleep physiology has made huge strides in recent years, uncovering the neurological structures which are critical to sleep regulation. However, given the small number of species studied in such detail in the laboratory, it remains to be seen how universal these mechanisms are across the whole mammalian order. Mammalian sleep is extremely diverse, and the unihemispheric sleep of dolphins is nothing like the rapidly cycling sleep of rodents, or the single daily block of humans. Here, we use a mathematical model to demonstrate that the established sleep physiology can indeed account for the sleep of a wide range of mammals. Furthermore, the model gives insight into why the sleep patterns of different species are so distinct: smaller animals burn energy more rapidly, resulting in more rapid sleep–wake cycling. We also show that mammals that sleep unihemispherically may have a single additional neuronal pathway which prevents sleep-promoting neurons on opposite sides of the hypothalamus from activating simultaneously. These findings suggest that the basic physiology controlling sleep evolved before mammals, and illustrate the functional flexibility of this simple system.


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