Brain responses to anticipatory cues and milkshake taste in obesity, and their relationship to bariatric surgery outcome

Marinka M G Koenis; Pavlos K Papasavas; Ronald J Janssen; Darren S Tishler; Godfrey D Pearlson

doi:10.1016/j.neuroimage.2021.118623

Brain responses to anticipatory cues and milkshake taste in obesity, and their relationship to bariatric surgery outcome

Neuroimage. 2021 Dec 15:245:118623. doi: 10.1016/j.neuroimage.2021.118623. Epub 2021 Oct 7.

Authors

Marinka M G Koenis¹, Pavlos K Papasavas², Ronald J Janssen³, Darren S Tishler², Godfrey D Pearlson⁴

Affiliations

¹ Olin Neuropsychiatry Research Center, Institute of Living at Hartford Hospital, 200 Retreat Avenue, Hartford, CT 06102, United States. Electronic address: maria.koenis@hhchealth.org.
² Division of Metabolic and Bariatric Surgery, Hartford Hospital, 80 Seymour Street, Hartford, CT 06102, United States.
³ Olin Neuropsychiatry Research Center, Institute of Living at Hartford Hospital, 200 Retreat Avenue, Hartford, CT 06102, United States.
⁴ Olin Neuropsychiatry Research Center, Institute of Living at Hartford Hospital, 200 Retreat Avenue, Hartford, CT 06102, United States; Department of Psychiatry, Yale University School of Medicine, 333 Cedar Street, New Haven, CT 06510, United States; Department of Neuroscience, Yale University School of Medicine, 333 Cedar Street, New Haven, CT 06510, United States.

Abstract

There is substantial variability in percent total weight loss (%TWL) following bariatric surgery. Functional brain imaging may explain more variance in post-surgical weight loss than psychological or metabolic information. Here we examined the neuronal responses during anticipatory cues and receipt of drops of milkshake in 52 pre-bariatric surgery men and women with severe obesity (OW, BMI = 35-60 kg/m²) (23 sleeve gastrectomy (SG), 24 Roux-en-Y gastric bypass (RYGB), 3 laparoscopic adjustable gastric banding (LAGB), 2 did not undergo surgery) and 21 healthy-weight (HW) controls (BMI = 19-27 kg/m²). One-year post-surgery weight loss ranged from 3.1 to 44.0 TWL%. Compared to HW, OW had a stronger response to milkshake cues (compared to water) in frontal and motor, somatosensory, occipital, and cerebellar regions. Responses to milkshake taste receipt (compared to water) differed from HW in frontal, motor, and supramarginal regions where OW showed more similar response to water. One year post-surgery, responses to high-fat milkshake cues normalized in frontal, motor, and somatosensory regions. This change in brain response was related to scores on a composite health index. We found no correlation between baseline response to milkshake cues or tastes and%TWL at 1-yr post-surgery. In RYGB participants only, a stronger response to low-fat milkshake and water cues (compared to high-fat) in supramarginal and cuneal regions respectively was associated with more weight loss. A stronger cerebellar response to high-fat vs low-fat milkshake receipt was also associated with more weight loss. We confirm differential responses to anticipatory milkshake cues in participants with severe obesity and HW in the largest adult cohort to date. Our brain wide results emphasizes the need to look beyond reward and cognitive control regions. Despite the lack of a correlation with post-surgical weight loss in the entire surgical group, participants who underwent RYGB showed predictive power in several regions and contrasts. Our findings may help in understanding the neuronal mechanisms associated with obesity.

Keywords: Bariatric surgery; Obesity; Reward; Weight loss; fMRI.

Publication types

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

MeSH terms

Adolescent
Adult
Aged
Bariatric Surgery*
Beverages*
Cues*
Female
Humans
Image Processing, Computer-Assisted
Magnetic Resonance Imaging / methods*
Male
Middle Aged
Neuroimaging / methods*
Obesity, Morbid / surgery*
Reward*
Taste*
Visual Perception
Weight Loss

Grants and funding

R01 DK113408/DK/NIDDK NIH HHS/United States