What is it about?

Sleep continues to perplex scientists and researchers. Despite decades of sleep research, we still lack a clear understanding of the biological functions and evolution of sleep. In this review, we will examine sleep from a functional and phylogenetic perspective and describe some important conceptual gaps in understanding sleep. Classical theories of the biology and evolution of sleep emphasize sensory activation, energy balance, and metabolic homeostasis. Advances in electrophysiology, functional neuroimaging, and neuroplasticity allow us to view sleep within the framework of neural dynamics. With this paradigm shift, we have come to realize the importance of neurodynamic homeostasis in shaping the biology of sleep. Evidently, animals sleep to achieve neurodynamic and metabolic homeostasis. We are not aware of any framework for understanding sleep where neurodynamic, metabolic, homeostatic, chronophasic, and afferent variables are all taken into account. This motivated us to propose the two-mode three-drive (2m3d) paradigm of sleep. In the 2m3d paradigm, local neurodynamic/metabolic (N/M) processes switch between two modes—m0 andm1—in response to three drives—afferent, chronophasic, and homeostatic. The spatiotemporal integration of local m0/m1 operations gives rise to the global states of sleep and wakefulness. As a framework of evolution, the 2m3d paradigm allows us to view sleep as a robust adaptive strategy that evolved so animals can periodically reinforce neurodynamic and metabolic homeostasis while remaining sensitive to their internal and external environment.

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Why is it important?

Sleep remains enigmatic in regards to its biological function and evolution. It is generally accepted that sleep is essential for metabolic homeostasis and functional recovery, defense and response to injury, neuroplasticity and neurodynamic homeostasis, and timing of biological processes. However, the phenotypic diversity in animal sleep suggests that each sleep function may vary in importance from one animal species to another. Some aquatic mammals, many birds, and perhaps some reptiles engage in unihemispheric sleep. Fish that constantly swim and birds that constantly fly give the impression of ‘not sleeping’ but it is not clear whether these animals attenuate their sleep, sleep in short bouts, engage in unihemispheric sleep, or forego sleep entirely. Changes in the functional anatomy of sleep during evolution stand in stark contrast to the conservation of sleep molecular mechanisms. The latter serves as motivation to search for a unifying principle for sleep function and evolution. Theoretical frameworks that attempt to explain sleep function or evolution emphasize certain aspects of biology, such as energy balance, homeostasis, neurodynamics, and the interaction of a few variables. Despite the fact that sleep is a global state emerging from the interaction of neurodynamic, metabolic, homeostatic, chronophasic, and afferent variables, current theories and models for understanding sleep take some, not all, of these variables into account. This motivated us to propose the two-mode three-drive (2m3d) paradigm—a mental framework for understanding sleep function and evolution where all these variables are taken into account and integrated in space and time.

Perspectives

• Sleep is vital for homeostasis, restitution, defense, plasticity, and bioperiodicity. • Animal sleep is phenotypically diverse. • Sleep molecular mechanisms are highly conserved in evolution. • Theories of sleep function and evolution emphasize different aspects of biology. • The 2m3d paradigm may help solve the enigmas of sleep biology and evolution.

Dr Edward C. Mader
Louisiana State University

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This page is a summary of: Sleep as spatiotemporal integration of biological processes that evolved to periodically reinforce neurodynamic and metabolic homeostasis: The 2m3d paradigm of sleep, Journal of the Neurological Sciences, August 2016, Elsevier,
DOI: 10.1016/j.jns.2016.05.025.
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