Influence of sucrose ingestion on brainstem and hypothalamic intrinsic oscillations in lean and obese women.
OBJECTIVE
The study of intrinsic fluctuations in the blood oxygen level-dependent signal of functional magnetic resonance imaging can provide insight into the effect of physiologic states on brain processes. In an effort to better understand the brain-gut communication induced by the absorption and metabolism of nutrients in healthy lean and obese individuals, we investigated whether ingestion of nutritive and non-nutritive sweetened beverages differentially engages the hypothalamus and brainstem vagal pathways in lean and obese women.


METHODS
In a 2-day, double-blind crossover study, 11 lean and 11 obese healthy women underwent functional magnetic resonance imaging scans after ingestion of 2 beverages of different sucrose content, but identical sweetness. During scans, subjects rested with eyes closed.


RESULTS
Blood oxygen level-dependent fluctuations demonstrated significantly greater power in the highest frequency band (slow-3: 0.073-0.198 Hz) after ingestion of high-sucrose compared with low-sucrose beverages in the nucleus tractus solitarius for both groups. Obese women had greater connectivity between the right lateral hypothalamus and a reward-related brain region and weaker connectivity with homeostasis and gustatory-related brain regions than lean women.


CONCLUSIONS
In a functional magnetic resonance imaging study, we observed sucrose-related changes in oscillatory dynamics of blood oxygen level-dependent fluctuations in brainstem and hypothalamus in lean and obese women. The observed frequency changes are consistent with a rapid vagally mediated mechanism due to nutrient absorption, rather than sweet taste receptor activation. These findings provide support for altered interaction between homeostatic and reward networks in obese individuals.
Gail and Gerald Oppenheimer Family Center for Neurobiology of Stress, David Geffen School of Medicine, Los Angeles, California; Department of Medicine, Division of Digestive Diseases, University of California, Los Angeles, California. Electronic address: lakilpatrick@mednet.ucla.edu.
Lisa A
LA
Kilpatrick
Gail and Gerald Oppenheimer Family Center for Neurobiology of Stress, David Geffen School of Medicine, Los Angeles, California.
Kristen
K
Coveleskie
Gail and Gerald Oppenheimer Family Center for Neurobiology of Stress, David Geffen School of Medicine, Los Angeles, California; Department of Medicine, Division of Digestive Diseases, University of California, Los Angeles, California.
Lynn
L
Connolly
Gail and Gerald Oppenheimer Family Center for Neurobiology of Stress, David Geffen School of Medicine, Los Angeles, California; Department of Medicine, Division of Digestive Diseases, University of California, Los Angeles, California; Ahmanson-Lovelace Brain Mapping Center, Los Angeles, California; Brain Research Institute, University of California, Los Angeles, Los Angeles, California.
Jennifer S
JS
Labus
Gail and Gerald Oppenheimer Family Center for Neurobiology of Stress, David Geffen School of Medicine, Los Angeles, California; Department of Medicine, Division of Digestive Diseases, University of California, Los Angeles, California.
Bahar
B
Ebrat
Gail and Gerald Oppenheimer Family Center for Neurobiology of Stress, David Geffen School of Medicine, Los Angeles, California; Department of Medicine, Division of Digestive Diseases, University of California, Los Angeles, California.
Jean
J
Stains
Gail and Gerald Oppenheimer Family Center for Neurobiology of Stress, David Geffen School of Medicine, Los Angeles, California; Department of Medicine, Division of Digestive Diseases, University of California, Los Angeles, California.
Zhiguo
Z
Jiang
Gail and Gerald Oppenheimer Family Center for Neurobiology of Stress, David Geffen School of Medicine, Los Angeles, California; Department of Medicine, Division of Digestive Diseases, University of California, Los Angeles, California.
Brandall Y
BY
Suyenobu
Department of Anatomy, Physiology, and Cell Biology, School of Veterinary Medicine, University of California, Davis, Davis, California.
Helen E
HE
Raybould
Gail and Gerald Oppenheimer Family Center for Neurobiology of Stress, David Geffen School of Medicine, Los Angeles, California; Department of Medicine, Division of Digestive Diseases, University of California, Los Angeles, California.
Kirsten
K
Tillisch
Gail and Gerald Oppenheimer Family Center for Neurobiology of Stress, David Geffen School of Medicine, Los Angeles, California; Department of Medicine, Division of Digestive Diseases, University of California, Los Angeles, California; Ahmanson-Lovelace Brain Mapping Center, Los Angeles, California; Department of Psychiatry, University of California, Los Angeles, Los Angeles, California; Brain Research Institute, University of California, Los Angeles, Los Angeles, California.
Emeran A
EA
Mayer
D000284:Administration, Oral; D000328:Adult; D001628:Beverages; D001931:Brain Mapping / Q000379:methods; D001933:Brain Stem / Q000378:metabolism / Q000503:physiopathology*; D018592:Cross-Over Studies; D019422:Dietary Sucrose / Q000008:administration & dosage* / Q000378:metabolism; D004311:Double-Blind Method; D005260:Female; D006706:Homeostasis; D006801:Humans; D007031:Hypothalamus / Q000378:metabolism / Q000503:physiopathology*; D008279:Magnetic Resonance Imaging; D009765:Obesity / Q000378:metabolism / Q000503:physiopathology* / Q000523:psychology; D009991:Oscillometry; D010100:Oxygen / Q000097:blood; D012201:Reward; D012527:Satiation; D013851:Thinness / Q000378:metabolism / Q000503:physiopathology* / Q000523:psychology; D013997:Time Factors; D014630:Vagus Nerve / Q000503:physiopathology; D055815:Young Adult
D019422:Dietary Sucrose; D010100:Oxygen
Food Intake; Obesity; Resting State; Satiety