Acute Sleep Deprivation Enhances the Brain's Response to Hedonic Food Stimuli: An fMRI Study

Department of Neuroscience, Uppsala University, Box 593, SE-751 24 Uppsala, Sweden.
The Journal of Clinical Endocrinology and Metabolism (Impact Factor: 6.21). 03/2012; 97(3):E443-7. DOI: 10.1210/jc.2011-2759
Source: PubMed


There is growing recognition that a large number of individuals living in Western society are chronically sleep deprived. Sleep deprivation is associated with an increase in food consumption and appetite. However, the brain regions that are most susceptible to sleep deprivation-induced changes when processing food stimuli are unknown.
Our objective was to examine brain activation after sleep and sleep deprivation in response to images of food.
Twelve normal-weight male subjects were examined on two sessions in a counterbalanced fashion: after one night of total sleep deprivation and one night of sleep. On the morning after either total sleep deprivation or sleep, neural activation was measured by functional magnetic resonance imaging in a block design alternating between high- and low-calorie food items. Hunger ratings and morning fasting plasma glucose concentrations were assessed before the scan, as were appetite ratings in response to food images after the scan.
Compared with sleep, total sleep deprivation was associated with an increased activation in the right anterior cingulate cortex in response to food images, independent of calorie content and prescan hunger ratings. Relative to the postsleep condition, in the total sleep deprivation condition, the activation in the anterior cingulate cortex evoked by foods correlated positively with postscan subjective appetite ratings. Self-reported hunger after the nocturnal vigil was enhanced, but importantly, no change in fasting plasma glucose concentration was found.
These results provide evidence that acute sleep loss enhances hedonic stimulus processing in the brain underlying the drive to consume food, independent of plasma glucose levels. These findings highlight a potentially important mechanism contributing to the growing levels of obesity in Western society.

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Available from: Christian Benedict, Mar 27, 2015
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    • "Hence, the investigation of sleep following acute, isocaloric aerobic and resistance exercise is warranted. Studies also reported greater neuronal responsiveness to food versus non-food stimuli following imposed sleep restrictions (Benedict et al., 2012; St-Onge et al., 2012). It is, however, unknown whether habitual changes in sleep parameters under free-living conditions are associated with changes in food reward. "
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    ABSTRACT: This study examined the effects of acute, isocaloric aerobic and resistance exercise on different sleep parameters, and whether changes in these sleep parameters between sessions were related to next morning food reward. Fourteen men and women (age: 21.9 ± 2.7 years; body mass index: 22.7 ± 1.9 kg m−²) participated in three randomized crossover sessions: aerobic exercise; resistance exercise; and sedentary control. Target exercise energy expenditure was matched at 4 kcal kg−1 of body weight, and performed at 70% of VO2peak or 70% of 1 repetition-maximal. Sleep was measured (accelerometry) for 22 h following each session. The ‘wanting’ for visual food cues (validated computer task) was assessed the next morning. There were no differences in sleep parameters and food ‘wanting’ between conditions. Decreases in sleep duration and earlier wake-times were significantly associated with increased food ‘wanting’ between sessions (P = 0.001). However, these associations were no longer significant after controlling for elapsed time between wake-time and the food reward task. These findings suggest that shorter sleep durations and earlier wake-times are associated with increased food reward, but these associations are driven by elapsed time between awakening and completion of the food reward task.
    Full-text · Article · Jan 2015 · Journal of Sleep Research
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    • "Their fed state was confirmed using self-reported, perceived hunger status rather than providing a standardized meal before the scan. Although providing a standardized meal could minimize the influence of hunger status on task performance [119, 120], it could also introduce a confounding factor; that is, "liking" or "disliking" the meal. Examining potential differences in neural responses due to eating standardized versus normal meals prior to scanning should be conducted in future studies. "
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    ABSTRACT: Background The loss of self-control or inability to resist tempting/rewarding foods, and the development of less healthful eating habits may be explained by three key neural systems: (1) a hyper-functioning striatum system driven by external rewarding cues; (2) a hypo-functioning decision-making and impulse control system; and (3) an altered insula system involved in the translation of homeostatic and interoceptive signals into self-awareness and what may be subjectively experienced as a feeling. Methods The present study examined the activity within two of these neural systems when subjects were exposed to images of high-calorie versus low-calorie foods using functional magnetic resonance imaging (fMRI), and related this activity to dietary intake, assessed by 24-hour recall. Thirty youth (mean BMI = 23.1 kg/m2, range = 19.1 - 33.7; age =19.7 years, range = 14 - 22) were scanned using fMRI while performing food-specific go/nogo tasks. Results Behaviorally, participants more readily pressed a response button when go trials consisted of high-calorie food cues (HGo task) and less readily pressed the response button when go trials consisted of low-calorie food cues (LGo task). This habitual response to high-calorie food cues was greater for individuals with higher BMI and individuals who reportedly consume more high-calorie foods. Response inhibition to the high-calorie food cues was most difficult for individuals with a higher BMI and individuals who reportedly consume more high-calorie foods. fMRI results confirmed our hypotheses that (1) the "habitual" system (right striatum) was more activated in response to high-calorie food cues during the go trials than low-calorie food go trials, and its activity correlated with participants’ BMI, as well as their consumption of high-calorie foods; (2) the prefrontal system was more active in nogo trials than go trials, and this activity was inversely correlated with BMI and high-calorie food consumption. Conclusions Using a cross-sectional design, our findings help increase understanding of the neural basis of one’s loss of ability to self-control when faced with tempting food cues. Though the design does not permit inferences regarding whether the inhibitory control deficits and hyper-responsivity of reward regions are individual vulnerability factors for overeating, or the results of habitual overeating.
    Full-text · Article · Sep 2014 · Nutrition Journal
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    • "Considering that GLP-1 infusion increases postprandial satiety in normal weight7 as well as obese humans,14 a delay in the postprandial GLP-1 response might affect food intake regulation and in particular impact inter-meal snacking that has been shown to be augmented after sleep loss.4, 15 Accordingly, our group has demonstrated that TSD enhances the brain's response to high-calorie food stimuli presented after a caloric preload.16 The tentative conclusion that alterations in postprandial GLP-1 dynamics might contribute to such effects of sleep loss is supported by findings in rats that the GLP-1 analog exendin-4 decreases the rewarding value of food.17 "
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    ABSTRACT: Objective: Previous experiments have demonstrated that acute sleep loss impairs glucose homeostasis and increases food intake in humans. The incretin hormone glucagon-like peptide 1 (GLP-1) enhances postprandial insulin secretion and promotes satiety. Hypothesizing that the detrimental metabolic effects of sleep curtailment imply alterations in GLP-1 signaling, we investigated 24-h serum total GLP-1 concentrations during total sleep deprivation and a normal sleep/wake cycle (comprising ~8 hours of sleep) in 12 healthy young men. Methods: Sessions started at 1800 h, and subjects were provided with standardized meals. Assessments of serum GLP-1 took place in 1.5- to 3-h intervals, focusing on the response to breakfast intake (3.8 MJ). Results: Across conditions, 24-h concentration profiles of GLP-1 were characterized by the expected postprandial increases (P<0.001). While there were no differences in magnitude between conditions (P>0.11), the postprandial GLP-1 peak response to breakfast intake was delayed by approximately 90 min following sleep loss in comparison to regular sleep (P<0.02). Conclusions: Results indicate that acute total sleep deprivation exerts a mild, but discernible effect on the postprandial dynamics of circulating GLP-1 concentrations in healthy men.
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