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Review
. 2016 Oct 24;26(20):R1073-R1087.
doi: 10.1016/j.cub.2016.08.068.

Unraveling the Evolutionary Determinants of Sleep

Affiliations
Review

Unraveling the Evolutionary Determinants of Sleep

William J Joiner. Curr Biol. .

Abstract

Despite decades of intense study, the functions of sleep are still shrouded in mystery. The difficulty in understanding these functions can be at least partly attributed to the varied manifestations of sleep in different animals. Daily sleep duration can range from 4-20 hrs among mammals, and sleep can manifest throughout the brain, or it can alternate over time between cerebral hemispheres, depending on the species. Ecological factors are likely to have shaped these and other sleep behaviors during evolution by altering the properties of conserved arousal circuits in the brain. Nonetheless, core functions of sleep are likely to have arisen early and to have persisted to the present day in diverse organisms. This review will discuss the evolutionary forces that may be responsible for phylogenetic differences in sleep and the potential core functions that sleep fulfills.

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Figures

Figure 1
Figure 1. NREM and REM sleep are correlated with quantifiable ecological and physiological variables across evolution
Positive and negative correlations are marked accordingly. Measured variables are listed centrally in color, with the impacted hypothesis for sleep function listed immediately below in parentheses. Except for brain mass, which was correlated with percent REM sleep, all variables were correlated with NREM or REM sleep durations. The unlabeled bottom loop shows that NREM and REM sleep are positively correlated with each other. Only mammals were used in these studies [–51]. In cases in which one study was unable to detect a correlation, the positive outcome of another study is still shown based on the notion that correlations are inherently difficult to detect. Not shown: positive correlation between total sleep duration and ratio of cortical density to cortical surface area [75], which has been hypothesized to support a role for sleep in metabolic clearance from the brain [74].
Figure 2
Figure 2. Conserved neurotransmitter systems that control sleep
Colored circles represent pharmacological, histological or genetic confirmation of the existence of neurotransmitter systems in mice, zebrafish and flies. The invertebrate neurotransmitter equivalent of norepinephrine is octopamine. Question marks label neurotransmitter systems that have not yet been tested for roles in regulating sleep in zebrafish. X indicates that in flies the single known adenosine receptor does not regulate sleep, though it does not exclude the possible involvement of additional adenosine receptors that have yet to be identified.
Figure 3
Figure 3. Neuroanatomical pathways by which neurotransmitter systems regulate arousal in the mammalian brain
The cell bodies of each neurotransmitter system are located in brain regions whose names are colored and abbreviated as follows: BF (basal forebrain), LH (lateral hypothalamus), TMN (tuberomamillary nucleus), DR (dorsal raphe nucleus), VTA (ventral tegmental area), LC (locus coeruleus), LDT/PPT (laterodorsal tegmental and pedunculopontine nuclei). Not shown: GABAergic inhibition of most of these brain regions by the ventrolateral preoptic nucleus to promote sleep. During waking, the cortex is excited by ventral and dorsal pathways through the basal forebrain and thalamus, respectively. During REM sleep, aminergic signaling is reduced, thus blocking sensory throughput at the level of the thalamus, but the persistence of cholinergic signaling through the ventral pathway continues to excite the cortex. During NREM sleep, aminergic and cholinergic signaling are both reduced, leading to lowered cortical activation, the appearance of SWA, and its entrainment by thalamocortical loops. Yellow and pink areas represent the forebrain and brainstem, respectively.
Figure 4
Figure 4. Cladogram of proposed evolutionary relationships across the animal kingdom
Red lines represent clades in which NREM and REM sleep have been detected by EEG. Pink lines represent taxa in which both sleep states are expected based on relatedness to taxa in red. Purple lines represent taxa with uncertain sleep outcomes. Blue lines represent taxa in which multiple features of sleep have been confirmed but neither NREM nor REM sleep has been detected. Evolutionary relationships were replotted from [193, 209, 210].
Figure 5
Figure 5. Homology between vertebrates and invertebrates in neuroanatomical control of arousal
(A) The basic circuit for vertebrate arousal involves aminergic excitation of the ventral forebrain and thalamus, which in turn excite the cortex. This circuit is well-established in mammals and is probably similar in birds and reptiles. Arousal-controlling nuclei are also found in homologous locations in fish, but in these animals the thalamus projects to the limbic system, including the brain region that is thought to function like the mammalian hippocampus. Thus, fish do not possess the thalamocortical loops that allow for entrainment of SWA, and in fact this form of NREM sleep has not been detected in fish. Instead it is possible that hippocampal sharp wave ripples, which have been detected in fish, serve a rudimentary related function. (B) A homologous circuit can be found in insects and other invertebrates that possess mushroom bodies (MBs), which are believed to be derived from an ancestral circuit that gave rise to the vertebrate cerebral cortex. Like the cortex, MBs also undergo oscillations that are thought to be important for memory. Abbreviations: DP (dorsal pallium); DVR (dorsal ventricular ridge); 5HT (serotonin); DA (dopamine); NA (noradrenaline or its invertebrate equivalent, octopamine).

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