Energetic theories of sleep function

A three part series on the function of sleep, considering three different types of models. I'm currently working on a thesis, and this is a snippet from that work.

One of the oldest proposals regarding the functional purpose of sleep is the role sleep plays in organizing behavior in a way to optimize energy expenditure; even a minor saving in energy expenditure could be preserved evolutionarily. At times optimal for action as determined by circadian factors and resource availability, waking function peaks (Mignot, 2008). This preserves energy while food would not be available, or the organism is not best suited for going about waking affairs, such as restricting hunting behavior to a time of day most optimal for vision. This would suggest, as observed, that sleep would have the strongest restrictive effect on animals most dependent upon these processes, while having a less restrictive effect on grazers and browsers (Hobson, 2005). With the brain as an incredibly energy-intensive organ, it would be a primary target of this process.

One point of benefit that these theories have is the link between circadian disruption and metabolic malfunction (Kohsaka & Bass, 2007). Further, mechanisms underlying feeding behavior have strong associations with the orexin system underlying the flip-flop switch (Saper, 2006). The primary proposed biochemical correlate in this model is adenosine, primarily released as a metabolite from glial cells (Benington & Heller, 1995). Adenosine has been found to increase after sleep deprivation, and serves as an inhibitory signal for cholinergic basal forebrain nuclei (McCarley & Massaquoi, 1992).

Unfortunately, this model leaves far too much unexplained. Although adenosine clearly serves a function in regulating sleep homeostasis in mammals, it’s far from clear how sleep energetically benefits the organism. The observations that local cell populations can enter synchronous firing indicative of sleep (Vyazovkiy et al., 2011) in addition to instances of unihemispheric sleep (Mukhametov et al., 1977) call into question any model that focuses too heavily on the functionality of sleep as being at the scale of the whole brain or whole organism. Also, regarding the diminished sleep of browsers and grazers, it still would seem unusual that sleep has not been totally eliminated in animals which would seemingly be suited for consuming throughout the 24-hour cycle.

Perhaps even more pressing are issues related to the energetics of sleep itself. Sleep is a very active process; although some energy is conserved during NREM sleep, some mammals have a much more efficient way of energy conservation: hibernation. Marked by a lowering of the core body temperature to a few degrees above ambient temperature, as well as incredibly slowed metabolic rate and dampened neural activity (Heller & Ruby, 2004), hibernation is an excellent tool for energy conservation. Were the primary function of sleep energetic in nature, it would much more closely resemble hibernation than it currently does (Mignot, 2008). Animals coming out of hibernation also experience sleep rebound, as if deprived of sleep during the time spent in hibernation (Heller & Ruby, 2004), which would not be expected if the two processes had overlapping functionality.

The model is also incredibly specific to endothermic organisms. While the model may serve as an explanation of the conservation of sleep among high-metabolism small mammals (Mignot, 2008), it does little to explain sleep in reptiles, and even less to explain observed sleep-like states observed in flies and flatworms (Hendricks et al., 2000; Shaw et al., 2000; Raizen et al., 2008).

Lastly, mammalian REM sleep again poses a particular problem for this model. REM sleep is marked by increased energetic demands, with wake-like neural activity and increased breathing and heart rate (Parmeggiani, 2003). Whatever function served by REM sleep, by this approach, would seem to be disconnected entirely from non-REM sleep.

Sources:

Benington, J.H, & Heller, H.C. (1995) Restoration of brain energy metabolism as the function of sleep. Progress in Neurobiology 45: 347-360.

Heller, H.C. & Ruby, N.F. (2004) Sleep and circadian rhythms in mammalian torpor. Annual Reviews in Physiology 66: 275-289.

Hendricks, J.C., Finn, S.M., Panckeri, K.A., Chavkin, J., Williams, J.A., Sehgal, A., & Pack, A.I. (2000) Rest in Drosophila is a sleep-like state. Neuron 25:129-138.

Hobson, J.A. (2005) Sleep is of the brain, by the brain and for the brain. Nature 437:1254-1256.

Kohsaka, A. & Bass, J. (2007) A sense of time: How molecular clocks organize metabolism. Trends in Endocrinology and Metabolism 18: 4-11.

McCarley, R.W., & Massaquoi, S.G. (1992) Neurobiological structure of the revised limit cycle reciprocal interaction model of REM cycle control. Journal of Sleep Research 1: 132-137

Mignot, E. (2008) Why we sleep: The temporal organization of recovery. PLoS Biology 6(4): e106.

Mukhametov, L.M., Supin, A.Y., & Polyakova, I.G. (1977) Interhemispheric asymmetry of the electroencephalographic sleep patterns in dolphins. Brain Research 134:581-584.

Parmeggiani, P.L. (2003) Thermoregulation and sleep. Frontiers in Bioscience 8: s557-s567.

Raizen, D.M., Zimmerman, J.E., Maycock, M.H., Ta, U.D., You, Y.J., Sandaram, M.V., & Pack, A.I. (2008) Lethargus is a Caenorhabditis elegans sleep-like state. Nature 451:569-572.

Saper, C.B. (2006) Staying awake for dinner: Hypothalamic integration of sleep, feeding, and circadian rhythms. Progress in Brain Research 153: 243-252.

Shaw, P.J., Cirelli, C., Greenspan, R.J., Tononi, G. (2000) Correlates of sleep and waking in Drosophila melanogaster. Science 287:1834-1837.

Vyazovkiy, V.V., Olcese, U., Hanlon, E.C., Nir, Y., Cirelli, C., & Tononi, G. (2011) Local sleep in awake rats. Nature 472: 443-447