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

Vyazovskiy, Vladyslav V.; Cirelli, Chiara; Tononi, Giulio; Tobler, Irene

doi:10.1016/j.brainresbull.2007.10.040

Cited by 57 publications

(42 citation statements)

References 33 publications

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“…Beginning with the first quantitative study of brain circulation and metabolism prior to sleep in humans (Mangold et al 1955), 1 there have been a total of six additional studies in humans that we know of (Boyle et al 1994;Braun et al 1997;Buchsbaum et al 1989;Madsen et al 1991aMadsen et al , 1991bThomas et al 2000), one in monkeys (Kennedy et al 1982), one in cats (Reivich et al 1968), and one in mice (Vyazovskiy et al 2008). …”

Section: Discussionmentioning

confidence: 99%

“…Obviously, more work needs to be done that emphasizes a more comprehensive view of glucose metabolism. The idea of "local sleep" during wake (Vyazovskiy et al 2011) should also be considered.…”

Section: Discussionmentioning

confidence: 99%

“…An important corollary of this hypothesis is that an increase in synaptic density should boost the metabolic cost of brain function, because the majority of that cost originates in the synapses (for a recent review see Raichle and Mintun 2006). Despite an extant literature on quantitative measures of brain circulation and metabolism in relation to sleep in humans (Andersson et al 1998;Boyle et al 1994;Braun et al 1997;Buchsbaum et al 1989;Madsen et al 1991aMadsen et al , 1991bMangold et al 1955;Thomas et al 2003) and laboratory animals (Kennedy et al 1976;Reivich et al 1968;Vyazovskiy et al 2008), an adequate test of this cost-based hypothesis remains to be done.…”

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confidence: 99%

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Morning-evening variation in human brain metabolism and memory circuits

Shannon

Dosenbach

et al. 2013

Journal of Neurophysiology

103

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Prior LJ, Nolan TS, Snyder AZ, Raichle ME. Morning-evening variation in human brain metabolism and memory circuits. J Neurophysiol 109: 1444 -1456, 2013. First published November 28, 2012 doi:10.1152/jn.00651.2012.-It has been posited that a critical function of sleep is synaptic renormalization following a net increase in synaptic strength during wake. We hypothesized that wake would alter the resting-state functional organization of the brain and increase its metabolic cost. To test these hypotheses, two experiments were performed. In one, we obtained morning and evening resting-state functional MRI scans to assess changes in functional brain organization. In the second experiment, we obtained quantitative positron emission tomography measures of glucose and oxygen consumption to assess the cost of wake. We found selective changes in brain organization. Most prominently, bilateral medial temporal regions were locally connected in the morning but in the evening exhibited strong correlations with frontal and parietal brain regions involved in memory retrieval. We speculate that these changes may reflect aspects of memory consolidation recurring on a daily basis. Surprisingly, these changes in brain organization occurred without increases in brain metabolism.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

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Morning-evening variation in human brain metabolism and memory circuits

Shannon

Dosenbach

et al. 2013

Journal of Neurophysiology

103

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“…How the changes in brain and body metabolism that occur with changes in behavioral states relate to sleep function remains, however, unknown. So far, the evidence is based on glucose metabolism or gene expression related to metabolism of lipids and proteins (Kennedy et al, 1982;Everson et al, 1994;Cirelli and Tononi, 2000b;Netchiporouk et al, 2001;Franken et al, 2003;Brown, 2004;Mackiewicz et al, 2007;Vyazovskiy et al, 2008a). Changes in metabolism in living animals are regulated both locally (activitydependent) and globally through circulating humoral factors.…”

Section: Stimulation Of Cortical Cultures Induces Similar Changes In mentioning

confidence: 99%

Key Electrophysiological, Molecular, and Metabolic Signatures of Sleep and Wakefulness Revealed in Primary Cortical Cultures

et al. 2012

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Although sleep is defined as a behavioral state, at the cortical level sleep has local and use-dependent features suggesting that it is a property of neuronal assemblies requiring sleep in function of the activation experienced during prior wakefulness. Here we show that mature cortical cultured neurons display a default state characterized by synchronized burst-pause firing activity reminiscent of sleep. This default sleep-like state can be changed to transient tonic firing reminiscent of wakefulness when cultures are stimulated with a mixture of waking neurotransmitters and spontaneously returns to sleep-like state. In addition to electrophysiological similarities, the transcriptome of stimulated cultures strikingly resembles the cortical transcriptome of sleep-deprived mice, and plastic changes as reflected by AMPA receptors phosphorylation are also similar. We used our in vitro model and sleep-deprived animals to map the metabolic pathways activated by waking. Only a few metabolic pathways were identified, including glycolysis, aminoacid, and lipids. Unexpectedly large increases in lysolipids were found both in vivo after sleep deprivation and in vitro after stimulation, strongly suggesting that sleep might play a major role in reestablishing the neuronal membrane homeostasis. With our in vitro model, the cellular and molecular consequences of sleep and wakefulness can now be investigated in a dish.

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“…Wakefulness is a metabolic challenge for brain regions responsible for arousal (Porkka-Heiskanen et al, 2002;Cirelli, 2006;Vyazovskiy et al, 2008), and it has been suggested that during prolonged waking supplementary energy stores are used to sustain neuronal activity (Benington and Heller, 1995). Aging is associated with changes in sleep-wake architecture, including vigilance state fragmentation (i.e., the inability to maintain prolonged periods of wake and sleep), and attenuated homeostatic sleep response to sleep deprivation (Carskadon et al, 1982;Buysse et al, 1992;Ohayon et al, 2004;Cajochen et al, 2006).…”

Section: Introductionmentioning

confidence: 99%

Basal Forebrain Lactate Release and Promotion of Cortical Arousal during Prolonged Waking Is Attenuated in Aging

Wigren¹,

Rytkönen²,

Porkka‐Heiskanen³

2009

J. Neurosci.

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The wake-promoting basal forebrain (BF) is critically involved in sustaining cortical arousal. In the present study, we investigated how aging affects the capacity of the BF to cope with continuous activation during prolonged waking. Increased neuronal activity induces lactate release in the activated brain area, and BF stimulation increases cortical arousal. We used in vivo microdialysis to measure lactate levels in the BF, and electroencephalography (EEG) to measure cortical arousal, during 3 h sleep deprivation (SD) in three age groups of rats. Lactate increased during SD in young but not in aged (middle-aged and old) rats. The increase in high-frequency (HF) EEG theta power (7-9 Hz), a marker of cortical arousal and active waking, was attenuated in the aged. Furthermore, a positive correlation between BF lactate release and HF EEG theta increase was found in young but not in aged rats. We hypothesized that these age-related attenuations result from reduced capacity of the BF to respond to increased neuronal activation. This was tested by stimulating the BF with glutamate receptor agonist NMDA. Whereas BF stimulation increased waking in young and old rats, lactate increase and the HF EEG theta increase were attenuated in the old. Also, the homeostatic increase in sleep intensity after SD was attenuated in aged rats. Our results suggest that an age-related attenuation in BF function reduces cortical arousal during prolonged waking. As the quality of waking is important in regulating the subsequent sleep, reduced cortical arousal during SD may contribute to the age-related reduction in sleep intensity.

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

Cited by 57 publications

References 33 publications

Morning-evening variation in human brain metabolism and memory circuits

Morning-evening variation in human brain metabolism and memory circuits

Key Electrophysiological, Molecular, and Metabolic Signatures of Sleep and Wakefulness Revealed in Primary Cortical Cultures

Basal Forebrain Lactate Release and Promotion of Cortical Arousal during Prolonged Waking Is Attenuated in Aging

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