Olfactory connectivity mediates sleep-dependent food choices in humans

Sleep deprivation has marked effects on food intake, shifting food choices toward energy-dense options. Here we test the hypothesis that neural processing in central olfactory circuits, in tandem with the endocannabinoid system (ECS), plays a key role in mediating this relationship. We combined a pa...

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Main Authors: Surabhi Bhutani, James D Howard, Rachel Reynolds, Phyllis C Zee, Jay Gottfried, Thorsten Kahnt
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2019-10-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/49053
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spelling doaj-e33552d54da4499aaf3ab2866cf59a772021-05-05T17:59:09ZengeLife Sciences Publications LtdeLife2050-084X2019-10-01810.7554/eLife.49053Olfactory connectivity mediates sleep-dependent food choices in humansSurabhi Bhutani0James D Howard1https://orcid.org/0000-0002-9309-3773Rachel Reynolds2Phyllis C Zee3Jay Gottfried4Thorsten Kahnt5https://orcid.org/0000-0002-3575-2670Department of Neurology, Feinberg School of Medicine, Northwestern University, Chicago, United States; School of Exercise and Nutritional Sciences, College of Health and Human Services, San Diego State University, San Diego, United StatesDepartment of Neurology, Feinberg School of Medicine, Northwestern University, Chicago, United StatesDepartment of Neurology, Feinberg School of Medicine, Northwestern University, Chicago, United StatesDepartment of Neurology, Feinberg School of Medicine, Northwestern University, Chicago, United StatesDepartment of Neurology, Feinberg School of Medicine, Northwestern University, Chicago, United States; Department of Neurology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, United States; Department of Psychology, School of Arts and Sciences, University of Pennsylvania, Philadelphia, United StatesDepartment of Neurology, Feinberg School of Medicine, Northwestern University, Chicago, United States; Department of Psychiatry and Behavioral Sciences, Feinberg School of Medicine, Northwestern University, Chicago, United States; Department of Psychology, Weinberg College of Arts and Sciences, Northwestern University, Evanston, United StatesSleep deprivation has marked effects on food intake, shifting food choices toward energy-dense options. Here we test the hypothesis that neural processing in central olfactory circuits, in tandem with the endocannabinoid system (ECS), plays a key role in mediating this relationship. We combined a partial sleep-deprivation protocol, pattern-based olfactory neuroimaging, and ad libitum food intake to test how central olfactory mechanisms alter food intake after sleep deprivation. We found that sleep restriction increased levels of the ECS compound 2-oleoylglycerol (2-OG), enhanced encoding of food odors in piriform cortex, and shifted food choices toward energy-dense food items. Importantly, the relationship between changes in 2-OG and food choices was formally mediated by odor-evoked connectivity between the piriform cortex and insula, a region involved in integrating feeding-related signals. These findings describe a potential neurobiological pathway by which state-dependent changes in the ECS may modulate chemosensory processing to regulate food choices.https://elifesciences.org/articles/49053sleep deprivationfood intakeolfactionfMRI
collection DOAJ
language English
format Article
sources DOAJ
author Surabhi Bhutani
James D Howard
Rachel Reynolds
Phyllis C Zee
Jay Gottfried
Thorsten Kahnt
spellingShingle Surabhi Bhutani
James D Howard
Rachel Reynolds
Phyllis C Zee
Jay Gottfried
Thorsten Kahnt
Olfactory connectivity mediates sleep-dependent food choices in humans
eLife
sleep deprivation
food intake
olfaction
fMRI
author_facet Surabhi Bhutani
James D Howard
Rachel Reynolds
Phyllis C Zee
Jay Gottfried
Thorsten Kahnt
author_sort Surabhi Bhutani
title Olfactory connectivity mediates sleep-dependent food choices in humans
title_short Olfactory connectivity mediates sleep-dependent food choices in humans
title_full Olfactory connectivity mediates sleep-dependent food choices in humans
title_fullStr Olfactory connectivity mediates sleep-dependent food choices in humans
title_full_unstemmed Olfactory connectivity mediates sleep-dependent food choices in humans
title_sort olfactory connectivity mediates sleep-dependent food choices in humans
publisher eLife Sciences Publications Ltd
series eLife
issn 2050-084X
publishDate 2019-10-01
description Sleep deprivation has marked effects on food intake, shifting food choices toward energy-dense options. Here we test the hypothesis that neural processing in central olfactory circuits, in tandem with the endocannabinoid system (ECS), plays a key role in mediating this relationship. We combined a partial sleep-deprivation protocol, pattern-based olfactory neuroimaging, and ad libitum food intake to test how central olfactory mechanisms alter food intake after sleep deprivation. We found that sleep restriction increased levels of the ECS compound 2-oleoylglycerol (2-OG), enhanced encoding of food odors in piriform cortex, and shifted food choices toward energy-dense food items. Importantly, the relationship between changes in 2-OG and food choices was formally mediated by odor-evoked connectivity between the piriform cortex and insula, a region involved in integrating feeding-related signals. These findings describe a potential neurobiological pathway by which state-dependent changes in the ECS may modulate chemosensory processing to regulate food choices.
topic sleep deprivation
food intake
olfaction
fMRI
url https://elifesciences.org/articles/49053
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