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Cortical metabolic rates as measured by 2-deoxyglucose-uptake are increased after waking and decreased after sleep in mice


Vyazovskiy, V V; Cirelli, C; Tononi, G; Tobler, I (2008). Cortical metabolic rates as measured by 2-deoxyglucose-uptake are increased after waking and decreased after sleep in mice. Brain Research Bulletin, 75(5):591-597.

Abstract

A recent hypothesis suggests that a major function of sleep is to renormalize synaptic changes that occur during wakefulness as a result of learning processes [G. Tononi, C. Cirelli, Sleep and synaptic homeostasis: a hypothesis, Brain Res. Bull. 62 (2003) 143-150; G. Tononi, C. Cirelli, Sleep function and synaptic homeostasis, Sleep Med. Rev. 10 (2006) 49-62]. Specifically, according to this synaptic homeostasis hypothesis, wakefulness results in a net increase in synaptic strength, while sleep is associated with synaptic downscaling. Since synaptic activity accounts for a large fraction of brain energy metabolism, one of the predictions of the hypothesis is that if synaptic weight increases in the course of wakefulness, cerebral metabolic rates should also increase, while the opposite would happen after a period of sleep. In this study we therefore measured brain metabolic rate during wakefulness and determined whether it was affected by the previous sleep-wake history. Three groups of mice in which behavioral states were determined by visual observation were subjected to 6h of sleep deprivation (SD). Group 1 was injected with 2-deoxyglucose (2-DG) 45 min before the end of SD, while Group 2 and Group 3 were injected with 2-DG after an additional period (2-3h) of waking or sleep, respectively. During the 45-min interval between 2-DG injection and sacrifice all mice were kept awake. We found that in mice that slept approximately 2.5h the 2-DG-uptake was globally decreased, on average by 15-20%, compared to the first two groups that were kept awake. On average, Group 2, which stayed awake approximately 2h more than Group 1, showed only a small further increase in 2-DG-uptake relative to Group 1. Moreover, the brain regions in which 2-DG-uptake increased the least when waking was prolonged by approximately 2h showed the most pronounced decrease in DG-uptake after sleep. The data are consistent with the prediction that sleep may reset cerebral metabolic rates to a lower level.

A recent hypothesis suggests that a major function of sleep is to renormalize synaptic changes that occur during wakefulness as a result of learning processes [G. Tononi, C. Cirelli, Sleep and synaptic homeostasis: a hypothesis, Brain Res. Bull. 62 (2003) 143-150; G. Tononi, C. Cirelli, Sleep function and synaptic homeostasis, Sleep Med. Rev. 10 (2006) 49-62]. Specifically, according to this synaptic homeostasis hypothesis, wakefulness results in a net increase in synaptic strength, while sleep is associated with synaptic downscaling. Since synaptic activity accounts for a large fraction of brain energy metabolism, one of the predictions of the hypothesis is that if synaptic weight increases in the course of wakefulness, cerebral metabolic rates should also increase, while the opposite would happen after a period of sleep. In this study we therefore measured brain metabolic rate during wakefulness and determined whether it was affected by the previous sleep-wake history. Three groups of mice in which behavioral states were determined by visual observation were subjected to 6h of sleep deprivation (SD). Group 1 was injected with 2-deoxyglucose (2-DG) 45 min before the end of SD, while Group 2 and Group 3 were injected with 2-DG after an additional period (2-3h) of waking or sleep, respectively. During the 45-min interval between 2-DG injection and sacrifice all mice were kept awake. We found that in mice that slept approximately 2.5h the 2-DG-uptake was globally decreased, on average by 15-20%, compared to the first two groups that were kept awake. On average, Group 2, which stayed awake approximately 2h more than Group 1, showed only a small further increase in 2-DG-uptake relative to Group 1. Moreover, the brain regions in which 2-DG-uptake increased the least when waking was prolonged by approximately 2h showed the most pronounced decrease in DG-uptake after sleep. The data are consistent with the prediction that sleep may reset cerebral metabolic rates to a lower level.

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Additional indexing

Item Type:Journal Article, refereed, original work
Communities & Collections:04 Faculty of Medicine > Institute of Pharmacology and Toxicology
04 Faculty of Medicine > Center for Integrative Human Physiology
Dewey Decimal Classification:570 Life sciences; biology
610 Medicine & health
Language:English
Date:28 March 2008
Deposited On:01 Dec 2008 10:07
Last Modified:05 Apr 2016 12:35
Publisher:Elsevier
ISSN:0361-9230
Publisher DOI:10.1016/j.brainresbull.2007.10.040
PubMed ID:18355635
Permanent URL: http://doi.org/10.5167/uzh-5979

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