Greater striatopallidal adaptive coding during cue–reward learning and food reward habituation predict future weight gain

• Published in: NeuroImage (Orlando, Fla.) Fla.), 2014-10, Vol.99, p.122-128
• Main Authors: Burger, Kyle S., Stice, Eric
• Format: Article
• Language: English
• Subjects: Adolescent; Biological and medical sciences; Body Mass Index; Body Weight - physiology; Cues; Cue–reward learning; Female; fMRI; Food; Food reward habituation; Fundamental and applied biological sciences. Psychology; Globus Pallidus - physiology; Habituation, Psychophysiologic - physiology; Humans; Incentive salience; Learning - physiology; Magnetic Resonance Imaging; Medical research; Medical sciences; Metabolic diseases; Neostriatum - physiology; Obesity; Obesity risk factors; Pavlovian conditioning; Reward; Risk Factors; Rodents; Studies; Vertebrates: nervous system and sense organs; Weight control; Weight Gain - physiology
• ISSN: 1053-8119; 1095-9572
• DOI: 10.1016/j.neuroimage.2014.05.066

Animal experiments indicate that after repeated pairings of palatable food receipt and cues that predict palatable food receipt, dopamine signaling increases in response to predictive cues, but decreases in response to food receipt. Using functional MRI and mixed effects growth curve models with 35 females (M age=15.5±0.9; M BMI=24.5±5.4) we documented an increase in BOLD response in the caudate (r=.42) during exposure to cues predicting impending milkshake receipt over repeated exposures, demonstrating a direct measure of in vivo cue–reward learning in humans. Further, we observed a simultaneous decrease in putamen (r=−.33) and ventral pallidum (r=−.45) response during milkshake receipt that occurred over repeated exposures, putatively reflecting food reward habitation. We then tested whether cue–reward learning and habituation slopes predicted future weight over 2-year follow-up. Those who exhibited the greatest escalation in ventral pallidum responsivity to cues and the greatest decrease in caudate response to milkshake receipt showed significantly larger increases in BMI (r=.39 and −.69 respectively). Interestingly, cue–reward learning propensity and food reward habituation were not correlated, implying that these factors may constitute qualitatively distinct vulnerability pathways to excess weight gain. These two individual difference factors may provide insight as to why certain people have shown obesity onset in response to the current obesogenic environment in western cultures, whereas others have not. •Differences in cue–reward learning and habituation may relate to food intake.•Individual differences in these phenomena haven't been studied in vivo in humans.•Propensity for cue–reward learning in the pallidum predicted future weight gain.•Propensity for food reward habituation in the caudate predicted future weight gain.•These processes appeared to be orthogonal, suggesting independent risk factors.