Upregulation of Gene Expression in Reward-Modulatory Striatal Opioid Systems by Sleep Loss

Epidemiological studies have shown a link between sleep loss and the obesity 'epidemic,' and several observations indicate that sleep curtailment engenders positive energy balance via increased palatable-food 'snacking.' These effects suggest alterations in reward-modulatory brai...

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Bibliographic Details
Published in:Neuropsychopharmacology (New York, N.Y.) N.Y.), 2013-12, Vol.38 (13), p.2578-2587
Main Authors: BALDO, Brian A, HANLON, Erin C, OBERMEYER, William, BREMER, Quentin, PALETZ, Elliott, BENCA, Ruth M
Format: Article
Language:English
Subjects:
Animals
Biological and medical sciences
Body Weight
Eating
Energy
Enkephalins - genetics
Enkephalins - metabolism
Fasting - physiology
Food
Gene expression
Insulin - blood
Leptin - blood
Male
Medical sciences
Medicine
Metabolism
Narcotics
Neostriatum - metabolism
Nerve Tissue Proteins - genetics
Nerve Tissue Proteins - metabolism
Neuroimaging
Neuropeptide Y - genetics
Neuropeptide Y - metabolism
Obesity
Opioid Peptides - genetics
Opioid Peptides - metabolism
Original
Peptides
Protein Precursors - genetics
Protein Precursors - metabolism
Public health
Rats
Rats, Sprague-Dawley
Research parks
Reward
Rodents
Sleep deprivation
Sleep Deprivation - pathology
Up-Regulation - physiology
Weight control
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Summary:Epidemiological studies have shown a link between sleep loss and the obesity 'epidemic,' and several observations indicate that sleep curtailment engenders positive energy balance via increased palatable-food 'snacking.' These effects suggest alterations in reward-modulatory brain systems. We explored the effects of 10 days of sleep deprivation in rats on the expression of striatal opioid peptide (OP) genes that subserve food motivation and hedonic reward, and compared effects with those seen in hypothalamic energy balance-regulatory systems. Sleep-deprived (Sleep-Dep) rats were compared with yoked forced-locomotion apparatus controls (App-Controls), food-restricted rats (Food-Restrict), and unmanipulated controls (Home-Cage). Detection of mRNA levels with in situ hybridization revealed a subregion-specific upregulation of striatal preproenkephalin and prodynorhin gene expression in the Sleep-Dep group relative to all other groups. Neuropeptide Y (NPY) gene expression in the hippocampal dentate gyrus and throughout neocortex was also robustly upregulated selectively in the Sleep-Dep group. In contrast, parallel gene expression changes were observed in the Sleep-Dep and Food-Restrict groups in hypothalamic energy-sensing systems (arcuate nucleus NPY was upregulated, and cocaine- and amphetamine-regulated transcript was downregulated), in alignment with leptin suppression in both groups. Together, these results reveal a novel set of sleep deprivation-induced transcriptional changes in reward-modulatory peptide systems, which are dissociable from the energy-balance perturbations of sleep loss or the potentially stressful effects of the forced-locomotion procedure. The recruitment of telencephalic food-reward systems may provide a feeding drive highly resistant to feedback control, which could engender obesity through the enhancement of palatable feeding.
ISSN:0893-133X
1740-634X
DOI:10.1038/npp.2013.174