Food Intake Recruits Orosensory and Post-ingestive Dopaminergic Circuits to Affect Eating Desire in Humans

Sharmili Edwin Thanarajah; Heiko Backes; Alexandra G DiFeliceantonio; Kerstin Albus; Anna Lena Cremer; Ruth Hanssen; Rachel N Lippert; Oliver A Cornely; Dana M Small; Jens C Brüning; Marc Tittgemeyer

doi:10.1016/j.cmet.2018.12.006

Food Intake Recruits Orosensory and Post-ingestive Dopaminergic Circuits to Affect Eating Desire in Humans

Cell Metab. 2019 Mar 5;29(3):695-706.e4. doi: 10.1016/j.cmet.2018.12.006. Epub 2018 Dec 27.

Authors

Affiliations

¹ Max Planck Institute for Metabolism Research, Cologne, Germany; Department of Neurology, University Hospital of Cologne, Cologne, Germany.
² Max Planck Institute for Metabolism Research, Cologne, Germany. Electronic address: backes@sf.mpg.de.
³ Max Planck Institute for Metabolism Research, Cologne, Germany; Department of Psychiatry, Yale University School of Medicine, New Haven, CT, USA; Modern Diet and Physiology Research Center, New Haven, CT, USA; Department of Neuroscience, Icahn School of Medicine at Mount Sinai, New York, NY, USA.
⁴ Cologne Cluster of Excellence in Cellular Stress and Aging-Associated Disease (CECAD), Cologne, Germany.
⁵ Max Planck Institute for Metabolism Research, Cologne, Germany.
⁶ Max Planck Institute for Metabolism Research, Cologne, Germany; Center for Endocrinology, Diabetes and Preventive Medicine (CEPD), University Hospital of Cologne, Cologne, Germany.
⁷ Cologne Cluster of Excellence in Cellular Stress and Aging-Associated Disease (CECAD), Cologne, Germany; Department I of Internal Medicine, University Hospital of Cologne, Cologne, Germany; Clinical Trials Centre Cologne (ZKS Köln), University of Cologne, Cologne, Germany.
⁸ Department of Psychiatry, Yale University School of Medicine, New Haven, CT, USA; Department of Psychology, Yale University, New Haven, CT, USA; Modern Diet and Physiology Research Center, New Haven, CT, USA.
⁹ Max Planck Institute for Metabolism Research, Cologne, Germany; Cologne Cluster of Excellence in Cellular Stress and Aging-Associated Disease (CECAD), Cologne, Germany; Center for Endocrinology, Diabetes and Preventive Medicine (CEPD), University Hospital of Cologne, Cologne, Germany.
¹⁰ Max Planck Institute for Metabolism Research, Cologne, Germany; Cologne Cluster of Excellence in Cellular Stress and Aging-Associated Disease (CECAD), Cologne, Germany; Modern Diet and Physiology Research Center, New Haven, CT, USA.

PMID: 30595479
DOI: 10.1016/j.cmet.2018.12.006

Abstract

Pleasant taste and nutritional value guide food selection behavior. Here, orosensory features of food may be secondary to its nutritional value in underlying reinforcement, but it is unclear how the brain encodes the reward value of food. Orosensory and peripheral physiological signals may act together on dopaminergic circuits to drive food intake. We combined fMRI and a novel [11C]raclopride PET method to assess systems-level activation and dopamine release in response to palatable food intake in humans. We identified immediate orosensory and delayed post-ingestive dopamine release. Both responses recruit segregated brain regions: specialized integrative pathways and higher cognitive centers. Furthermore, we identified brain areas where dopamine release reflected the subjective desire to eat. Immediate dopamine release in these wanting-related regions was inversely correlated with, and presumably inhibited, post-ingestive release in the dorsal striatum. Our results highlight the role of brain and periphery in interacting to reinforce food intake in humans.

Keywords: dopamine release; food reward; gut-brain axis; human brain; positron emission tomography; post-ingestive signaling; wanting.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Adult
Aged
Brain / metabolism*
Dopamine / metabolism*
Eating / physiology*
Food Preferences / physiology*
Healthy Volunteers
Humans
Magnetic Resonance Imaging / methods
Male
Middle Aged
Taste / physiology*

Substances

Dopamine