Olfactory connectivity mediates sleep-dependent food choices in humans

Author:

Bhutani Surabhi12,Howard James D1ORCID,Reynolds Rachel1,Zee Phyllis C1,Gottfried Jay134,Kahnt Thorsten156ORCID

Affiliation:

1. Department of Neurology, Feinberg School of Medicine, Northwestern University, Chicago, United States

2. School of Exercise and Nutritional Sciences, College of Health and Human Services, San Diego State University, San Diego, United States

3. Department of Neurology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, United States

4. Department of Psychology, School of Arts and Sciences, University of Pennsylvania, Philadelphia, United States

5. Department of Psychiatry and Behavioral Sciences, Feinberg School of Medicine, Northwestern University, Chicago, United States

6. Department of Psychology, Weinberg College of Arts and Sciences, Northwestern University, Evanston, United States

Abstract

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.

Funder

National Institute of Diabetes and Digestive and Kidney Diseases

National Institute on Deafness and Other Communication Disorders

National Center for Advancing Translational Sciences

National Heart, Lung, and Blood Institute

Publisher

eLife Sciences Publications, Ltd

Subject

General Immunology and Microbiology,General Biochemistry, Genetics and Molecular Biology,General Medicine,General Neuroscience

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