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Sleep as spatiotemporal integration of biological processes that evolved to periodically reinforce neurodynamic and metabolic homeostasis: The 2m3d paradigm of sleep

      Highlights

      • 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.

      Abstract

      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 and m1—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.

      Keywords

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