Sleep deprivation selectively up-regulates an amygdala-hypothalamic circuit involved in food reward

Abstract

Sleep loss is associated with increased obesity risk, as demonstrated by correlations between sleep duration and change in body mass index or body fat percentage. Whereas previous studies linked this weight gain to disturbed endocrine parameters after sleep deprivation (SD) or restriction, neuroimaging studies revealed up-regulated neural processing of food rewards after sleep loss in reward-processing areas such as the anterior cingulate cortex, ventral striatum and insula. To tackle this ongoing debate between homeostatic versus hedonic factors underlying sleep loss-associated weight gain, we rigorously tested the association between SD and food cue processing using high-resolution fMRI and assessment of hormones. After taking blood samples from thirty-two lean, healthy men, they underwent fMRI while performing a neuroeconomic, value-based decision making task with snack food and trinket rewards following a full night of habitual sleep (HS) and a night of SD in a repeated-measures cross-over design. We found that des-acyl ghrelin concentrations were increased after SD compared with HS. Despite similar hunger ratings due to fasting in both conditions, participants were willing to spend more money on food items only after SD. Furthermore, fMRI data paralleled this behavioral finding, revealing a food reward-specific up-regulation of hypothalamic valuation signals and amygdala-hypothalamic coupling after a single night of SD. Behavioral and fMRI results were not significantly correlated with changes in acyl, des-acyl or total ghrelin concentrations. Our results indicate that increased food valuation after sleep loss is due to hedonic rather than hormonal mechanisms.